Facile and versatile modification of cotton fibers for persistent antibacterial activity and enhanced hygroscopicity

Facile and Versatile Modi fication of Cotton Fibers for Persistent Antibacterial Activity and Enhanced Hygroscopicity Qiuquan Cai,† Shuliang Yang,‡ Chao Zhang,† Zimeng Li,‡ Xiaodong Li,*,

Facile and Versatile Modi fication of Cotton Fibers for Persistent Antibacterial Activity and Enhanced Hygroscopicity

Qiuquan Cai,† Shuliang Yang,‡ Chao Zhang,† Zimeng Li,‡ Xiaodong Li,*,‡ Zhiquan Shen,†

and Weipu Zhu*,†,§

†MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, People ’s Republic of China

‡Department of Oral and Maxillofacial Surgery, A ffiliated Stomatology Hospital, School of Medicine, Zhejiang University, Hangzhou

310006, China

§Key Laboratory of Adsorption and Separation Materials & Technologies of Zhejiang Province, Hangzhou 310027, China

*S Supporting Information

ABSTRACT: Natural fibers with functionalities have

at-tracted considerable attention However, developing facile and

versatile strategies to modify natural fibers is still a challenge.

In this study, cotton fibers, the most widely used natural

fibers, were partially oxidized by sodium periodate in aqueous

solution, to give oxidized cotton fibers containing multiple

aldehyde groups on their surface Then poly(hexamethylene

guanidine) was chemically grafted onto the oxidized cotton

fibers forming Schiff bases between the terminal amines of

poly(hexamethylene guanidine) and the aldehyde groups of

oxidized cotton fibers Finally, carbon−nitrogen double bonds

were reduced by sodium cyanoborohydride, to bound poly(hexamethylene guanidine) covalently to the surface of cotton fibers These functionalized fibers show strong and persistent antibacterial activity: complete inhibition against Escherichia coli and Staphylococcus aureus was maintained even after 1000 consecutive washing in distilled water On the other hand, cotton fibers with only physically adsorbed poly(hexamethylene guanidine) lost their antibacterial activity entirely after a few washes According to Cell Counting Kit-8 assay and hemolytic analysis, toxicity did not signi ficantly increase after chemical modi fication Attributing to the hydrophilicity of poly(hexamethylene guanidine) coatings, the modified cotton fibers were also more hygroscopic compared to untreated cotton fibers, which can improve the comfort of the fabrics made of modified cotton fibers This study provides a facile and versatile strategy to prepare modified polysaccharide natural fibers with durable antibacterial activity, biosecurity, and comfortable touch.

KEYWORDS: antibacterial, biocompatibility, cotton fiber, hygroscopicity, PHMG

■ INTRODUCTION

Cotton is one of the most important natural resources to

produce fabrics for clothing and other textile materials The

adhesion and growth of bacteria in cotton fabrics not only lead

to the performance degradation of cotton fabrics, but also

result in bacterial infection in human beings.1 Therefore,

antibacterial finishing of cotton fibers (CF) has created great

interest in laboratory research and industrial applications.2

Silver nanoparticles (Ag NPs) with high speci fic surface area,

strong antibacterial activity, and low cost can easily be

prepared from water-soluble silver salts, which can in situ

deposit on the surface of CF, resulting in antibacterial CF.3−10

Moreover, many other metal NPs, such as copper,11−14

zinc,15−20 and titanium,21−23 have also been employed as

antibacterial agents to modify CF These inorganic NPs serve

as leachable biocides that can be released from CF to kill the

surrounding bacteria However, CF coated with leachable

biocides are usually lacking in durable antibacterial activity

after long-term use because of the limited loading content.24,25 Hence, long-lasting antibacterial CF may play an important role in improving antibacterial e fficiency, preventing infections, and protecting human health.

Cationic polymers containing cationic groups and hydro-phobic groups are another kind of important synthetic biocides.26−33 Cationic polymers can be adsorbed onto the anionic membrane of bacteria by charge interactions Then their hydrophobic groups insert into the membrane and disrupt it, which leads to the death of bacteria.34 CF with covalently bonded cationic polymers can kill bacteria through a contact mechanism,35 which is quite di fferent from leachable biocides, resulting in CF with persistent antibacterial activity.36 Surface-initiated living/controlled radical polymerization of

Received: August 30, 2018 Accepted: October 11, 2018 Published: October 11, 2018

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cationic vinyl monomers from CF has been reported to

prepare antibacterial CF with stable polycation coating.37

Nevertheless, the potential application of this method is

hindered by the tedious reaction steps and critical

polymer-ization conditions Therefore, chemically grafting ready-made

cationic polymers onto CF seems to be an e fficient strategy for

preparing antibacterial CF, assuming the route can be

simpli fied.

Poly(hexamethylene guanidine) (PHMG) is an

environ-ment-friendly cationic polymer with strong antibacterial

activity and a low toxicity to human beings,38−42 which has

been widely used for water treatment,43 wound

disinfec-tion,44,45 food packing,46 and so on However, commercially

available linear PHMG with amine end groups cannot react

with the glucose units of cotton directly In order to solve this

problem, Guan et al synthesized a PHMG derivative with two

terminal epoxy groups by the polycondensation of PHMG with

poly(propylene glycol)diglycidyl ether , which then can be

chemically coated onto CF through hydroxyl −epoxy reaction

under alkaline conditions.1

In this study, we demonstrate a facile and versatile strategy

to covalently graft commercially available PHMG to CF

directly without any additional linker First, multiple aldehyde

functionalities are introduced to the surface of CF by

oxidization, which can react with the terminal amines of

PHMG in a high yield In the next step, the unstable Schi ff

base bonds between CF and PHMG were reduced into

carbon −nitrogen sigma bonds, greatly improving the stability

of PHMG coatings We further investigated the

biocompati-bility, antibacterial activity, moisture absorption, and retention

capacity of PHMG-coated CF.

■ EXPERIMENTAL SECTION

Materials CF (145.8 dtex of single yarn × 19 strands) was

purchased from Suzhou Shenchen Textiles Co Ltd., China PHMG

hydrochloride (Mn= 2100 g/mol, 99%) was obtained from Hubei

Xinyuan Shun Pharmaceutical Chemical Co Ltd., China Sodium

periodate (NaIO4, 99%, Aladdin, China), hydroxylamine

hydro-chloride (NH2OH·HCl, 99%, Aladdin, China), and sodium

cyanoborohydride (NaCNBH3, 99%, Alfa Aesar, USA) were used as

received Luria−Bertani (LB) broth, LB agar, and R2A agar were

purchased from Huankai Microbial Sci & Tech Co Ltd., China

Alpha-minimum essential medium (α-MEM) and fetal bovine serum

(FBS) were purchased from Invitrogen Co., USA The Cell Counting

Kit-8 was purchased from Sigma-Aldrich Chemicals, United States

Other reagents and solvents were of analytical grade and used as

received

Characterization All samples used for surface characterizations

were dried at 40 °C in vacuum prior to analysis The surface

morphologies of CF, oxidized CF (OCF), CF-g-PHMG, and

PHMG@CF were examined by scanning electron microscope

(SEM, SU-8010, Japan) after coating with platinum X-ray

photo-electron spectroscopy (XPS, VG ESCALAB MARK II, UK) and

energy dispersive X-ray (EDX) in the SEM system were used to

analyze the surface element composition of the samples Fourier

transform infrared attenuated total reflectance (FT-IR ATR)

spectrophotometer (Bruker Co TENSOR II, Germany) was used

to record the surface information Fluorescence images were collected

by afluorescence microscopy (Nikon Eclipse 80i, Japan) Tensile tests

were carried out by Instron-3343 tester with a stretching speed of 10

mm/min at room temperature The fiber samples (original gauge

length: 50 mm) were tested to determine the breaking tenacity (N/

tex) and elongation at break (%).1H NMR spectroscopy was carried

out by using a Bruker Avance-400 NMR spectrometer (400 MHz)

Preparation of OCF 0.2 g of NaIO4(0.94 mmol) was dissolved

in 100 mL deionized water and transferred into a 250 mL three-neck

round-bottomflask CF (2 g) was then charged into the flask under continuous magnetic stirring and nitrogen gasflow The oxidation of

CF was carried out at 35°C in dark conditions for a preset oxidation time Finally, the resultant OCF was ultrasonically washed with ethanol and deionized water three times sequentially and dried at 40

°C under vacuum for 12 h The oxidation degree of OCF, referring to the percentage of cellulose units that have been oxidized, was further determined by titration.47Typically, 100 mL hydroxylamine hydro-chloride methanol solution (20 mg/mL) and 1 g of OCF were charged into a 250 mL conicalflask followed by adding a drop of thymol blue ethanol solution (0.1%) as an indicator The mixture was stirred for 10 min until it turned pink It was then titrated with standard sodium hydroxide solution (0.03 mol/L) until the solution turned yellow and did not fade within 30 s The degree of oxidation (%) of OCF is calculated by

−

m

3

(1) where V2 and V1 (mL) are the volumes of the standard sodium hydroxide solution for the test groups and control groups, respectively C (mol/L) is the concentration of the standard sodium solution, m (g) is the weight of OCF, and M (g/mol) is the molecular weight of the cellulose unit (162 g/mol) Thefinal value of oxidation degree is an average of three parallel tests

Preparation of PHMG-Grafted CF (CF-g-PHMG) In a typical experiment, 3 g of PHMG (1.43 mmol) was charged into a 100 mL round-bottomflask with 30 mL deionized water to form a 100 mg/

mL aqueous solution of PHMG under continuous magnetic stirring Thereafter, 1 g of OCF was added into the solution Triethylamine (TEA; 0.1 mL) was added as the catalyst The aldehyde groups of OCF were reacted with the terminal amines of PHMG to give PHMG-grafted OCF (OCF-g-PHMG) through Schiff reaction under room temperature for 6 h Afterward, 0.5 g of NaCNBH3 (7.96 mmol) was added to the mixture for another 6 h of reaction to reduce the carbon−nitrogen double bonds into stable sigma bonds Finally, the sample was ultrasonically washed with ethanol and deionized water three times sequentially to remove the TEA, unreacted PHMG, and NaCNBH3 It was dried at 40°C in a vacuum oven to give CF-g-PHMG Conversion efficiency of aldehyde groups into Schiff base was determined by the hydroxylamine hydrochloride titration mentioned above The reaction efficiency of CHO (%) is calculated as follows

A

Reaction efficiency of CHO (%) 1 2 100

where A1 and A2 (mol/g) are the aldehyde contents of CF after oxidation and grafting, respectively The grafting density is defined as the percentage of the grafted cellulose units with respect to the total cellulose units of CF, which can be calculated from the following expression

Grafting density (%) reaction efficiency of CHO oxidation degree 100 (3) Preparation of CF with Physical Adsorption of PHMG (PHMG@CF) As a comparison, 1 g of CF was soaked in 100 mg/mL PHMG aqueous solution (30 mL) for 6 h Then, the sample was sequentially washed with ethanol and deionized water in an ultrasonic bath three times for 30 min and dried at 40°C under vacuum to give PHMG@CF

Antibacterial Assays The antibacterial activities of CF, OCF, CF-g-PHMG, and PHMG@CF were evaluated by measuring zones of inhibition, optical density at 600 nm [optical density (OD)600], as well as drop-plate methods The Escherichia coli and Staphylococcus aureus were used as model microorganisms The bacterial suspensions contained from 106 to 107 colony-forming units (CFU)/mL for all tests For the inhibition zone method, LB agar medium was prepared and autoclaved at 121°C for sterilization before use Then, 10 mL LB agar medium (as a liquid when cooled to 45°C) was mixed with an E

coli or S aureus broth to a concentration of 106CFU/mL and cast on

polystyrene Petri dishes Finally, each sterilizedfiber sample with a

coiled shape (0.5 g, 5 mm in diameter) was placed on the dish These

fiber samples were incubated at 37 °C for 24 h before observation

The zones of inhibition were recorded by a digital camera The OD600

measurement and drop-plate counting method were both adopted to

assess the antibacterial activities of thesefibers in liquid media For

the OD600measurement, 0.5 g of CF-g-PHMG was soaked in a 6-well

plate containing 10 mL of E coli or S aureus LB broth (106CFU/mL)

for each well and incubated at 37°C At different intervals (0, 3, 6, 9,

12, 24 h), 100μL of the cultured bacterial suspension was transferred

into a 96-well plate to measure the OD600 by a microplate

spectrophotometer (SpectraMax i3, USA) The inhibition ratio (%)

for bacteria is calculated by

i k

jjjjj j

y {

zzzzz z

sample negative

where ODsample, ODnegative, ODpositive, and ODblankare the absorbances

of sample with bacteria, sample only, bacteria only, and blank,

respectively Data are presented as the average± SD (n = 5)

For the drop-plate method, 0.5 g of CF-g-PHMG was soaked into a

6-well plate containing 10 mL E coli or S aureus LB broth (106CFU/

mL) for each well and incubated at 37°C At different intervals (0, 3,

6, 9, 12, 24 h), 100 μL of the cultured bacterial suspension was

transferred from each well and diluted to 10-fold serial dilutions The

optimal ranges of dilution times were 102to 105at 0 h, 104to 107at 3

h, and 105to 108after 6 h (6, 9, 12, 24 h), respectively 100μL of

each serial dilution was pulled up and expelled 10μL drops with each

push of the pipette onto one quadrant of an R2A agar plate that had

been divided into fourths and labeled for that particular dilution of the

sample Five drops of 10 μL were placed on the plated for each

dilution Then, the drops were let to soak into the media before

turning the plates for incubation at 37°C overnight The dilution

containing 3−30 colonies per 10 μL was counted after the colonies

had developed Viable bacteria counts are expressed as CFU/mL

according to the following formula48,49

V

Viable bacteria count (CFU/mL) average CFU dilution

p

(5) where Vpis volume plated (0.01 mL) Data are presented as average±

SD (n = 5)

Biocompatibility Evaluations Cytotoxicities of CF, OCF, and

CF-g-PHMG in vitro were assessed by the Cell Counting Kit-8

(CCK-8) assay Three kinds of cells, mouse osteoblastic cells

(MC3T3-E1), human breast adenocarcinoma cells (MCF-7), and

human breast cancer cells (Bcap-37), were used as model cells First,

an extract was obtained by impregnating 0.5 g offiber sample into 3

mLα-MEM, including 10% FBS at 37 °C for 24 h Then, the cell

broth was added into a 96-well plate and cultured in a humidified atmosphere of 5% CO2at 37°C for 24 h The extract was charged into the plate and incubated for another 24 h After incubation, the medium was removed carefully and replaced by the CCK-8 reagent and cultured for another 1 h Cell viability was determined by the OD

at 450 nm, which was measured by a microplate spectrophotometer The expression for cell viability (%) is as follows

sample blank

where ODsample, ODnegative, and ODblankare the absorbances of extract with cells, extract only, and blank, respectively Data are presented as the average± SD (n = 5) Hemolysis assay was conducted to evaluate the blood compatibility of CF, CF-g-PHMG, and PHMG@CF Human red blood cells (hRBCs) were obtained by venous puncture from healthy nonsmoking volunteers using standard blood-drawing procedures (normal bloodflow and no pressure) The present study was approved by the Ethics Committee of Zhejiang University Additionally, an informed consent was obtained from each healthy donor prior to obtaining blood The fresh hRBCs were washed with phosphate buffer saline (PBS), centrifuged three times, and diluted to 4% in volume with PBS Diluted hRBC suspension (2 mL) was charged into a 24-well plate containing 0.2 g of sterilized fiber samples The hRBC suspension with 0.9% saline and 0.1% Triton

X-100 served as the negative and positive groups, respectively The plates were cultured at 37°C for 1 h At last, the hRBC suspension was centrifuged under 3000 rpm and 4°C for 5 min The suspension (100μL) after centrifugation was transferred to a 96-well plate The

OD values at 576 nm were detected by a microplate spectropho-tometer The hemolysis (%) is calculated as follows

sample negative

where ODsample, ODnegative, and ODpositiveare the absorbances of the hRBCs suspension withfiber samples, 0.9% saline, and 0.1% Triton

X-100, respectively Data are presented as the average± SD (n = 5) Moisture Absorption and Retention Measurements The fiber samples were fully dried under vacuum in the presence of P2O5 before use Then they were placed in two different desiccators, where the internal relative humidity (RH) was kept at 43 and 81% by saturated K2CO3 and (NH4)2SO4 aqueous solutions at room temperature, respectively.50 The mass variation was measured at regular intervals The moisture absorption (%) was calculated by the percentage of weight increase of dry sample

W

where W1and W2(g) are the sample weights before and after placing into the desiccator with a certain humidity The moisture retention

Scheme 1 Preparation of CF-g-PHMG

capacity of the fibers was characterized by adding 1 g of the fiber

sample into a weighing bottle containing 0.1 g (10%) of deionized

water After the sample was fully wetted in the weighing bottle, it was

then placed into a desiccator filled with dry silica gels at room

temperature.50At regular intervals, the moisture retention (%) of the

sample is calculated by the percentage of residual water of wet sample

H

Moisture retention (%) 2 100

where H1and H2(g) are the sample weights before and after placing

into the desiccators The moisture absorption or retention over time

(W(t)) can be described by a Fick’s equation,51which for the case of

one-dimensional diffusion, takes the following form:

where A, B, and C are constants relative to thefibers and determined

from the nonlinearfitting of moisture absorption or retention data by

mathematical tools Further expression of the change rate of moisture

absorption or desorption is obtained from the derivative of moisture

absorption or retention

W

d

Ct

(11)

■ RESULTS AND DISCUSSION

Preparation and Characterization of CF-g-PHMG The

preparation routes of CF-g-PHMG are displayed in Scheme 1

Sodium periodate was employed as a mild oxidant to partly

convert the 2,3-vicinal hydroxyl groups of glucose units in the

CF into dialdehyde groups.52 In order to determine the

oxidation degree of hydroxyl groups, the amount of aldehyde

groups generated was measured by hydroxylamine

hydro-chloride titration The oxidation degree of CF varied over the

reaction process with oxidation time ( Figure 1 A) After 2 h of

oxidation, the oxidation degree quickly increased to the

maximum (2.55%), indicating that the hydroxyl groups of

CF were converted into aldehyde groups and reached a

corresponding maximal aldehyde content (315 μmol/g) for

OCF Interestingly, aldehyde content then decreased gradually

with oxidation time, which can be explained with the partly

dissolved dialdehyde cellulose because of chain scission.53The

OCF samples with various oxidation times were further grafted

with PHMG via Schi ff reaction to give OCF-g-PHMG The

reaction e fficiency of aldehyde groups (CHO) and global

grafting density of CF versus the oxidation time were also

measured by titration through the reaction of remaining CHO

with hydroxylamine hydrochloride, as shown in Figure 1 B.

OCF with the highest oxidation degree showed a highest

reaction e fficiency of aldehydes (32.6%), resulting in a highest

grafting density of 1.66% Finally, the carbon −nitrogen double

bonds and residual aldehyde groups of OCF-g-PHMG were

reduced to stable carbon −nitrogen sigma bonds and hydroxyl

groups The resultant CF-g-PHMG with highest grafting

density was used for further studies.

According to the photograph of CF, OCF, CF-g-PHMG,

and PHMG@CF ( Figure S1 ), macroscopic appearances of

these fibers did not significantly change after oxidizing,

grafting, and soaking SEM was further used to characterize

the surface morphologies of CF, OCF, CF-g-PHMG, and

PHMG@CF ( Figure 2 ) The surface of CF before grafting was

uniform and smooth, whereas that of OCF became coarse after

oxidation For CF-g-PHMG, a lot of filaments appeared on the

surface, which can be ascribed to the grafted PHMG segments.

However, PHMG@CF still showed smooth surfaces similar to

untreated CF because the physically adsorbed PHMG on the fiber surfaces cannot be maintained after washing several times Distribution of surface elements was imaged by the EDX mapping based on the C 1s, O 1s, and N 1s photoelectrons The overall contents of C, O, and N on the fiber surface can be

Figure 1.The oxidation degree (A), reaction efficiency of CHO, and grafting density (B) of CF vs oxidation time

Figure 2 SEM images and corresponding EDX mappings of CF, OCF, CF-g-PHMG, and PHMG@CF

counted from the EDX mapping (see Figure S2 ) Because the

content of O element in these four samples remains constant

according to the grafting mechanism, it can be used as a

standard to distinguish the di fference in the content of N

element before and after grafting The relative contents of

elements on PHMG@CF surface (58.5% C, 41.5% O, and 0%

N) were basically the same as those on CF and OCF surfaces

(for CF: 56.9% C, 43.1% O, and 0% N; for OCF: 56.3% C,

43.7% O, and 0% N), indicating that no PHMG existed on

their surfaces However, the overall compositions of the surface

element of CF-g-PHMG were 64.5% C, 31.7% O, and 3.8% N.

It was found by calculation that around 65% C and 100% O

derived from the CF raw materials, whereas 35% C and 100%

N accounted for the grafted PHMG The above results were

further con firmed by the detection of XPS As displayed in

Figure 3 , the peaks at the binding energy of 284, 397, and 531

eV can be assigned to the C 1s, N 1s, and O 1s photoelectrons,

respectively.54There were only two peaks of C and O from the

cellulose structure for CF After oxidation, the elemental

compositions on the surface of OCF did not signi ficantly

change compared to that of CF However, the new peak of N

element was detected for the CF-g-PHMG, demonstrating that

the PHMG was successfully grafted onto the surfaces of CF In

contrast, no peak of N element could be monitored from the

XPS spectrum of PHMG@CF, indicating that the physically

adsorbed PHMG had been entirely removed by washing.

More evidence of chemically grafting PHMG onto CF is

provided by FT-IR ATR spectroscopy and fluorescence

microscopy Figure S3 shows the FT-IR ATR spectra of CF,

OCF, CF-g-PHMG, and PHMG@CF In the FT-IR ATR

spectrum of CF-g-PHMG, a new characteristic peak of

guanidine groups appeared at 1630 cm−1, which proved that

PHMG was covalently bonded to the CF surface.55,56

However, no distinct di fference between the spectra of

untreated CF and PHMG@CF was observed Because the

PHMG is a cationic polymer, it can electrostatically adsorb

negatively charged fluorescein disodium salt, which can

identify the presence of PHMG on the surface.49 CF, OCF,

CF-g-PHMG, and PHMG@CF were dyed with an aqueous solution of fluorescein disodium salt (20 mg/mL) and washed

to remove the free salt In Figure S4 , as expected, only CF-g-PHMG showed green fluorescence under an excitation wavelength of 490 nm Overall, chemical bonding of PHMG onto the CF makes the coating more stable than that by soaking, and will not be eluted in water.

E ffects of chemical grafting of PHMG on the mechanical properties of fibers were investigated by tensile tests Figure S5 shows the stress −strain curves of CF, OCF, and CF-g-PHMG The strength unit of fibers used is specific stress, expressed as N/tex, which is de fined as the applied force (N) divided by its linear density (tex) of a yarn or fiber.57

It was found in the stress −strain curves that the breaking tenacity (breaking speci fic stress) of CF-g-PHMG (0.229 N/tex) were close to those of CF (0.238 N/tex) and OCF (0.232 N/tex) However, compared with the untreated CF, the elongation at break of OCF was slightly declined, which can be attributed to the slight chain scission of cellulose structure after oxidation Grafting of PHMG onto CF did not signi ficantly affect the elongation at the break of CF-g-PHMG These results indicate that CF-g-PHMG basically preserves the mechanical properties

of the untreated CF.

Antibacterial Activity of CF-g-PHMG The zones of inhibition were first conducted to verify the contacting antibacterial activities of modi fied CF.58

Surprisingly, CF-g-PHMG showed signi ficant inhibition zones larger than their contact areas for both E coli and S aureus ( Figure 4 A,B), which cannot be explained by the contact-kill mechanism In order to further investigate the antibacterial mechanism of CF-g-PHMG, 10 g of CF-g-PHMG was immersed in 1 L deionized water After ultrasonic washing for 12 h, the extract was lyophilized The resultant trace solid was dissolved in

DMSO-d6 for 1H NMR measurement As shown in Figure S6 , the signals of trace cellulose and PHMG were both detected in the spectrum.59We concluded that the very slow degradation of the cellulose backbone of CF-g-PHMG results in the di ffusion

of cellulose fragment with PHMG, which leads to the

Figure 3.XPS spectra of CF, OCF, CF-g-PHMG, and PHMG@CF

inhibition zones Thus, the antibacterial mechanism can be

attributed to the combination of the contact inhibition and

di ffusion inhibition On the one hand, the negative bacteria

membranes will be electrostatically attracted by the positive

surfaces of CF-g-PHMG Then the guanidine groups of

PHMG will disrupt the bacteria membranes, causing leakage

of cytoplasmic fluid and eventually killing the bacteria.35 , 60 − 62

On the other hand, the trace amount of degraded cellulose

with PHMG segments can kill bacteria that are free around the

fibers, resulting in extensive inhibitions zones Nevertheless,

without a cationic PHMG coating, CF, OCF, and PHMG@CF

did not exhibit any inhibition activities against the two kinds of

bacteria Although PHMG@CF can physically adsorb PHMG,

it loses its antibacterial activity after several washing cycles.

Inhibition e ffects of CF-g-PHMG against E coli and S aureus

were quanti fied by the OD600 method, as shown in Figure

4 C,D As expected, CF-g-PHMG showed e ffective antibacterial

activities against both E coli and S aureus, resulting in quite

low OD600values As summarized in Figure S7 , the inhibition

ratios of CF-g-PHMG against E coli after 12 and 24 h of

incubation were 92.9 and 95.6%, respectively Meanwhile,

those against S aureus after 12 and 24 h of incubation were

91.6 and 94.8%, respectively In contrast, the inhibition ratios

of other samples without a PHMG coating (CF, OCF, and

PHMG@CF) were no more than 7%, indicating that those

fibers did not affect the growth of bacteria.

Because the OD600method cannot distinguish dead bacteria

and living bacteria, the drop-plate method was further adopted

to count the living bacteria during the cultivation process As

shown in Figure 5 A,B, no living bacteria were found in the

plates for CF-g-PHMG even in the very beginning All bacteria

were killed after adding to the medium containing

CF-g-PHMG for a few minutes By contrast, CF, OCF, and

PHMG@CF exhibited the same trends of bacteria growth,

suggesting that these fibers do not have any antibacterial

capabilities These results can be easily observed from the

living-bacteria growth curves in Figure 5 C,D Consistent with

the measurements of OD600method, the bacteria growth could

not be suppressed during the whole cultivation process for CF, OCF, and PHMG@CF It was notable that living bacteria were counted to be 0 CFU/mL for CF-g-PHMG, indicating absolute inhibition of bacteria compared with the samples without PHMG coatings, with bacteria counts ranging from

108to 1010CFU/mL after 24 h of incubation.

The morphological changes in the bacteria grown on the surfaces of these fibers were observed by SEM ( Figure 6 ) The normal morphologies of living E coli and S aureus are rod shaped and spherical, respectively Without PHMG coatings, the bacteria on CF or OCF were numerous and structurally intact; that is, there are no apparent antibacterial activities for these fibers Although PHMG@CF was immersed with PHMG, the result showed that the bacteria can also grow normally on the surfaces after several cycles of washing As a comparison, few bacteria could be observed on the surfaces of CF-g-PHMG In addition, the walls of E coli or S aureus contacted with their surfaces were disrupted and deformed, as indicated by the white arrows in the images This suggests that these bacteria were killed by the coated cationic PHMG.

Figure 4.Inhibition zones of CF, OCF, CF-g-PHMG, and PHMG@

CF with E coli (A) and S aureus (B); OD600values of CF, OCF,

CF-g-PHMG, and PHMG@CF with E coli (C) and S aureus (D)

Figure 5.Drop-plate photographs of CF, OCF, CF-g-PHMG, and PHMG@CF with E coli (A) and S aureus (B); drop-plate counting of

CF, OCF, CF-g-PHMG, and PHMG@CF with E coli (C) and S aureus (D)

In order to study the durability of antibacterial e ffects,

CF-g-PHMG was ultrasonically washed with deionized water for

di fferent times (100, 200, 400, 600, 800, 1000) After drying,

the samples were further assessed by the zones of inhibition,

OD600 measurement, and drop-plate methods The bacterial

suspensions employed for the tests contained 106 CFU/mL.

The sizes of inhibition zones of CF-g-PHMG against E coli and

S aureus did not attenuate even after 1000 washing cycles

( Figure 7 A,B) The minimal inhibitory concentration of

PHMG is fairly low (2.5 −5 ppm);63

thus, a trace amount of degraded cellulose segments boned with PHMG is enough to kill the bacteria In addition, the inhibition ratios against E coli and S aureus did not signi ficantly compromise with an increase

in washing cycles from 10 (E coli 95.5% and S aureus 94.3%)

to 1000 (E coli 90.3% and S aureus 90.6%), as shown in Figure

7 C These results were recon firmed by the drop-plate method ( Figure 7 D) It can be clearly observed that no bacteria grew

on all of the plates for CF-g-PHMG (0 CFU/mL in the range from 101 to 104 times of dilutions), indicating that 100% antibacterial activities against E coli or S aureus were achieved even after 1000 consecutive washing cycles The reason for the long-lasting antibacterial activity of CF-g-PHMG is that the covalently bonded PHMG chains are reasonably stable Although a trace amount of PHMG was lost because of the slow degradation of cellulose during washing, enough PHMG grafts remained on the surface of CF even after 1000 washing cycles, demonstrating a durable antibacterial capability of CF-g-PHMG.

Biocompatibility of CF-g-PHMG In vitro cell viability assays of CF-g-PHMG with MC3T3-E1, MCF-7, and Bcap-37 cells were carried out to evaluate the biocompatibility of the modi fied fibers As displayed in Figure 8 , the viabilities of the

three kinds of cells did not signi ficantly decrease after oxidation and PHMG grafting, indicating the low toxicity of antibacterial

CF to living mammalian cells Unlike bacteria with negative charged membranes, the mammalian cell membranes usually present a lower net negative charge and have weak interactions with cations.64 It thus results in a low cytotoxicity of CF-g-PHMG toward the mammalian cells, which can be further con firmed by the following hemolytic analysis ( Figure S8 ) The hemolysis activity of CF-g-PHMG to hRBCs was less than 2%, which is similar to those of other samples without a PHMG coating (CF and PHMG@CF) Both cell viability assays and hemolytic analysis demonstrated an excellent biocompatibility of CF-g-PHMG.

Moisture Absorption and Retention of CF-g-PHMG The moisture absorption and retention capacities are critical to controlling the thermophysiological comfort of human body.65 Moisture absorption refers to the ability of fiber materials to absorb moisture from the humidi fied atmosphere The moisture absorption capacities of the fibers were determined

at two di fferent RH (43 and 81%) under room temperature, as shown in Figure 9 A,C CF-g-PHMG exhibited enhanced moisture absorption than untreated CF, which can improve the comfort of cotton fabrics.65−69Furthermore, the oxidation

Figure 6.SEM morphologies of E coli and S aureus on the surface of

CF, OCF, CF-g-PHMG, and PHMG@CF The lower images are the

enlargements of the rectangle area in the upper ones

Figure 7.Inhibition zones of CF-g-PHMG against E coli (A) and S

aureus (B), as well as the inhibition ratios (C) and drop-plate

photographs (D) of CF-g-PHMG after various washing frequencies

Figure 8.Cell viability of CF, OCF, and CF-g-PHMG by CCK-8 assays

of CF and soaking treatment of CF with PHMG solutions did

not significantly contribute to the increase in moisture

absorption capacity The introduction of hydrophilic guanidine

groups can account for the enhanced moisture absorption of

CF-g-PHMG Furthermore, the rates of moisture absorption of

the fibers were plotted from the derivatives of the fitting curves

of moisture absorption ( Figure 9 B,D), which represents the

change rates of moisture absorption per unit time

Interest-ingly, although the equilibrium moisture absorption of

CF-g-PHMG was higher under high RH (81%) than that under low

RH (43%), the initial rates of moisture absorption were close

under both RH At high RH, it took a long time for the rates of

moisture absorption of the fibers to reach their equilibrium.

As opposed to moisture absorption, the moisture retention

capability is de fined as the ability of fibers to retain their water

contents in dry conditions Moisture retention of samples is

presented in Figure 9 E The CF-g-PHMG showed the highest

level of moisture retention among these samples The balanced

rate of moisture retention of CF-g-PHMG was kept at 2.6%,

which can be ascribed to the hydration of the cationic PHMG.

The rate of moisture desorption was also obtained from the

derivative of the fitting curve of moisture retention ( Figure

9 F) Compared with CF, OCF, and PHMG@CF, the initial

rate of moisture desorption of CF-g-PHMG decreased by

around 40%, suggesting that CF-g-PHMG has good moisture

retention ability because of an enhanced interaction between

water and fiber surfaces Enhanced moisture retention of

CF-g-PHMG also contributes to the improvement of resistance to

bacteria adhesion and moisture permeability of clothes.69,70

Overall, the enhanced hygroscopicity of CF-g-PHMG can improve the clothing comfort and promote resistance to bacteria adhesion with the combination of inherent anti-bacterial activities.

■ CONCLUSIONS

We report a facile and versatile strategy to chemically graft PHMG onto CF directly via C −N sigma bonds The modified

CF shows strong and long-lasting antibacterial activity against both Gram-positive and Gram-negative bacteria even after

1000 cycles of washing The antibacterial mechanism mainly comes from the inhibition of covalent PHMG coating upon contact Moreover, the very slow degradation of cellulose bonded with PHMG leads to additional di ffusion inhibition The CF-g-PHMG also exhibited excellent biocompatibility based on CCK-8 and hemolytic assays Owing to the hydrophilicity of the PHMG coating, CF-g-PHMG possess enhanced moisture absorption and retention capacities compared with untreated CF, which can improve the comfort

of cotton fabrics This strategy can also be used to chemically modify other natural fibers with glucose units Functionalized natural fibers, which are easy to prepare, have persistent antibacterial activity, excellent biocompatibility, and comfort-able feel and have many potential applications in clothing and

as medical gauze.

Figure 9.Moisture absorption [(A,B) 43% RH; (C,D) 81% RH] and moisture retention (E,F) of CF, OCF, CF-g-PHMG, and PHMG@CF

■ ASSOCIATED CONTENT

*S Supporting Information

The Supporting Information is available free of charge on the

ACS Publications website at DOI: 10.1021/acsami.8b14986

Photograph and detailed characterizations of CF, OCF,

CF-g-PHMG, and PHMG@CF ( PDF )

■ AUTHOR INFORMATION

Corresponding Authors

*E-mail: cisarli@zju.edu.cn (X.L.).

*E-mail: zhuwp@zju.edu.cn (W.Z.).

ORCID

Weipu Zhu:0000-0002-6662-5543

Author Contributions

Q.C and S.Y contributed equally to this work The article was

written through contributions of all authors All authors have

given approval to the final version of the manuscript.

Notes

The authors declare no competing financial interest.

■ ACKNOWLEDGMENTS

W.Z acknowledges supports from National Natural Science

Foundation of China (21674094 and 21875209), Zhejiang

Provincial Natural Science Foundation of China

(LR18B040001), and Fundamental Research Funds for the

Central Universities (2017QNA4038).

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