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Volume 2020 | Article ID 7890215 | https://doi.org/10.1155/2020/7890215 Pankaj Kumar Tyagi | Cristina

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Chitosan-Reinforced MFC/NFC Aerogel and Antibacterial Culture Method-Dependent

Variation in the Sensitivity

Property
of Escherichia coli to Silver

Nanoparticles
Huanlei Yang,1 Shuxin Zhang,1 and Jinhua Yan 1

Show more R. Mariselvam | S.

Ignacimuthu | ... | P. Mosae
Academic Editor: Mingzhi Huang Selvakumar

Published: 26 Aug 2020

Biosynthesis and

Characterization of Silver

Abstract Nanoparticles Produced by

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using the reinforced aerogel. The excellent Ag-NP monodistribution on the aerogel was expressed by
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TEM. Both chitosan-reinforced Ag-NPs loaded MFC aerogel and NFC aerogel and expressed great
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antibacterial activity, though reinforced MFC aerogel exhibited better properties, like higher BET, lighter

density, more Ag-NP loading, and better distribution, than NFC aerogel in this research. Chitosan-

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reinforced MFC aerogel is a good potential substrate for nanoparticle loading and biocomposite making.
Green Synthesis,

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1. Introduction Reject All

CuO/ZnO Nanocomposite

Using Zingiber officinale

Aerogels are porous materials of interconnected nanostructures made from gels by replacing the liquid by

gas, which exhibit unusual properties, such as high porosity and surface area, low density, and low heat Rhizome Extract

conductivity [1]. A wide variety of aerogels have been reported in the literature. They can be produced

from silica, alumina, tin oxide, chromia, and carbon, with silica being the most widely used one [2]. The

unique properties associated with aerogels have led to their use in a wide range of applications such as

catalysts [2], catalyst supports [3], superthermal and sound insulators [2, 4], electronics, particle filters,

and as a storage media for gases in fuel cells [5, 6]. More recently, cellulose has gained interest as a

source material for the production of aerogels due to its renewability and biodegradability [7]. Cellulose

aerogels have proven particularly useful in applications where biocompatibility and biodegradability are

needed, such as for medicinal, cosmetic, and pharmaceutical applications, opening up the application

fields of aerogels even wider [8]. Micro/nanofibrillar cellulose (MFC/NFC) is isolated from natural

cellulose fibers by basically mechanical action after enzyme or chemical pretreatment. Its higher aspect

ratio made MFC/NFC an attractive application of providing a more beneficial template to accommodate

nanoparticles, for example, NFC with silver nanoparticles using UV reduction [9], NFC with magnetic

particles [10], and NFC with drug nanoparticles [11].

MFC/NFC aerogels generally can be prepared by two steps: one is the MFC/NFC suspension generated

by a unique method of enzymatic/chemical pretreatment and mechanical fibrillation by a microfluidizer

and the other is to produce aerogel by freezing the suspensions and dried in a special way [7, 12–15].
Different cellulose sources and preparation processes make the MFC/NFC cellulose aerogels with totally

different microstructures and properties [16, 17]. MFC/NFC has been widely investigated recently due to

its sustainable, renewable, and biocompatible nontoxic properties for relatively high physical-chemical

stability materials [18, 19]. The density and surface texture of the aerogels can be tuned by selecting the

concentration of the MFC/NFC dispersion before freeze-drying. All of these aerogels are based on the

hydrogen bond formation between MFC/NFCs [20]. Unfortunately, these hydrogen bonds can be easily

destroyed by immersing the aerogels in water, which limited the application of the aerogels [20].

Chemical cross-linking affords a method for the preparation of MFC/NFC cellulose aerogels with high

mechanical properties [21–23]. Although these efforts have been carried out for the improvement of the

mechanical properties of cellulose aerogels, the substances that can provide safe, renewable, and

biocompatible nontoxic properties are more desirable. Chitosan from the natural polymer chitin has good

biocompatibility, as well as extensive applications in pharmacology, biomedicine, agriculture, food, and

waste treatment [24]. Regarding the chemical nature, chitosan and cellulose have similar structures, with

the same β-glycosidic linkages, being the main difference as the presence of primary amino groups at

most of the C-2 positions in chitasan, instead of the hydroxyl groups. Much work has been devoted to the

study of chitosan blends with cellulose [25–28], poly(vinyl alcohol) [29–31], gelatin [32], collagen [33],

and others [34]. The evidence of some chitosan–cellulose chemical interactions was proved [19]. Our

group also reported that chitosan improved the nanopaper mechanical strength both in dry and wet states

by cross-linking [35]. That is, chitosan can be used as a cross-linker of cellulose and nanofibrils.

In the current work, we firstly reported chitosan-reinforced MFC/NFC aerogels and their application. The

aerogels showed improved mechanical properties. Using the reinforced aerogel as a template,

nanoparticles, silver as an example, were loaded uniformly.

2. Materials and Methods

2.1. MFC/NFC Preparation

Fully bleached eucalyptus pulp was passed through the microgrinder, 6 passes, at a concentration of

2.31%, to produce MFC suspension. Then some of the MFC suspension was treated by TEMPO before

passing the microfluidizer 10 times to produce NFC. The TEMPO oxidation technique was performed as

given in the literature with sodium hypochlorite as the terminal oxidant [36]. Dialysis was applied to

remove extra salts in NFC using Nomial MWCO 3500 (Fisherbrand regenerated cellulose) for 48 h with

Milli-Q water changing frequency every 5 h. The acidic group content of MFC and NFC was measured as

70 and 400 μmol/g, respectively, by titration as per the literature [37]. The titration steps were as follows:

0.01 M NaOH was added drop by drop till there was no further drop in system conductivity. Then the

amount of NaOH was recorded till the conductivity increased. The consumed NaOH can be calculated to

get the acidic group content. Both MFC and NFC ready-to-use slurries were kept in a refridgerator.

2.2. Chitosan Solution Preparation

Chitosan (MW 10253, viscosity 20 cP) was purchased from Aldrich (degree of deacetylation: ∼85%).

Chitosan solutions were prepared by dissolving chitosan (2% by weight) in (1% by volume) aqueous

acetic acid solution [38]. The solution was sonicated for 30 min before use.

2.3. MFC/NFC Aerogel Preparation

MFC/NFC dispersion with chitosan mixture at different ratios of 100/0, 90/10, 80/20, and 70/30 (MFC to

chitosan weight) was mixed to 0.5% by adding DI water, by using a high-shear mixer for 5 min, followed

by a magnetic bar stirring for 1 h, and then sonication for another 30 min. Then the mixture was

centrifuged to remove water at a speed of 1.2 × 104 rpm for 1 h. A gel was formed. The gel was frozen by

liquid nitrogen, then placed on a freeze dryer (Labconco) for at least 48 h. The properties of density,

strength, and BET surface area were examined. The density was measured by the volume and weight of

each aerogel. The strength was evaluated by its water stability which was conducted in water for stirring at

a given time. After Ag-NPs loaded, both the MFC/CH aerogel and NFC/CH aerogel BET surface areas

were measured after 4 h degassing at 105°C (Gemini VII Series surface area analyzer, Micromeritics

Instrument Corporation).

2.4. Nanoparticle Loading

The in situ loading of silver nanoparticles (Ag-NPs) onto the aerogels was carried out through the

reduction of 10 mM AgNO solution. Under ambient temperature (∼25°C), AgNO solution was absorbed
3 3

by the porous matrix by soaking or dropwise addition, keeping totally wet for enough time till the

aerogels are not absorbing solution anymore. After a certain time of air drying, a partially dehydrated

matrix was obtained. It was then immersed in an aqueous solution of NaBH (50 mM) for 20 min. The
4

color of the samples turned to yellow or dark brown due to the reduction of Ag + into silver nanoparticles.
The composite was rinsed with Milli-Q water three times to remove water-soluble substances and

unbound silver particles. Finally, the composite was freeze dried.

2.5. Aerogel Morphology

SEM sample preparation of the MFC/NFC slurry and aerogels with/without Ag-NPs : MFC/NFC (20 mL,

0.08%) was taken for magnetic stirring for 45 min, followed by 30 s sonication. A silicon plate was used

as the MFC/NFC material support. Firstly, the plate was cut into small pieces, which were soaked in 10%

NaOH solution for 30 s and then in Milli-Q water. These silicon pieces were dried by nitrogen blowing,

followed by UV exposure for 20 min. A tiny drop of the abovementioned MFC/NFC slurry was placed on

the surface of a cleaned silicon piece. Overnight air drying was needed before the SEM test. The samples

were coated with gold before SEM operation. The porous structures of MFC/NFC aerogels were

examined using a field emission scanning electron microscope (FESEM) at an accelerating voltage of 20

kV (a high resolution JEOL 6400F cold field emission SEM). The MFC/NFC aerogels with Ag-NPs were

characterized using VPSEM (Variable Pressure Scanning Electron Microscope, Hitachi S3200N) with an

energy dispersive X-ray spectrometer).

TEM preparation of MFC/NFC aerogels with Ag-NPs: A JEOL 2000FX transmission electron

microscope (TEM) operating at 20.0 kV was utilized to define the Ag-NPs in the MFC/NFC aerogels. A

specimen can be prepared by cutting the sample into thin slices using a diamond saw, then cutting 3-mm-

diameter disks from the slice, thinning the disk on a grinding wheel, dimpling the thinned disk, and then

ion milling it to electron transparency.

2.6. FTIR Spectroscopy

FTIR spectroscopy was performed on a PerkinElmer Spectrum (Version 10.03.09). Spectra were obtained
−1 −1
after the accumulation of 6 scans which had a resolution of 4 cm over the range of 4,000–650 cm .

2.7. Thermal Gravimetric Analysis (TGA)

In order to determine the thermal decomposition temperature of composite aerogels, thermogravimetric

analysis (TGA) was used. It was operated on Perkin Elmer TGA Q500 with a heating rate of 10°C/min to

500°C in a nitrogen atmosphere. In order to obtain the amount of Ag-NPs in aerogel, TGA under oxygen

in the range of 500–575°C was continued. The isothermal time for 25 min at 575°C was utilized.

2.8. Antibacterial Activity Test

The antibacterial activity of the aerogels was tested against Escherichia coli (E. coli), Gram-negative

bacteria, using the viable cell-counting method. Briefly, about 100 μL E. coli was cultivated in 100 mL of

a nutrient broth solution to give a bacterial concentration of about 7 × 1011 CFU/mL. Then, 1 mL of the

bacteria/nutrient solution was added to 9 mL of sterilized nutrient broth solution (0.8%). Several decimal

dilutions were performed until the bacterial concentration increased from 7 × 103 to 7 × 107 CFU/mL.

NFC, NFC/chitosan, and MFC/chitosan and their silver-loaded counterparts (NFC/chitosan/Ag-NPs and

MFC/chitosan/Ag-NPs) were used in the antibacterial tests. Accurate weight of the aerogel samples (100

mg) was assigned to the experiment. To perform the antibacterial testing, aerogels of the respective

samples were put into 10 mL of the bacteria/nutrient solution and incubated in a shaker at 37°C for 12 h.

After the exposure of the bacteria to films, 100 μL of the bacterial solution was taken out and quickly

spread on a plate containing nutrient agar. Plates containing bacteria were incubated at 37°C for 24 h, and

then the numbers of the surviving colonies were observed. These results were compared to the number of

bacterial colonies of the untreated control.

3. Results and Discussion

3.1. MFC/NFC Aerogel Physical Properties

MFC/NFC aerogels with chitosan addition were examined for their densities and strength. The dry

aerogel-retained stability in water is shown in Figure 1. MFC aerogels with 0% chitosan (A), 10%

chitosan (B), and 20% chitosan (C) were soaked into water and kept under magnetic stirring at 610 rpm

for 4 h. MFC aerogel with 0% chitosan was totally dispersed into water again, chitosan-added MFC

aerogels were kept intact. In addition, a 10% chitosan-added MFC aerogel compression test was

conducted for mechanical strength property of 0.36 MPa. The dry aerogel density was tested by

measuring the volume of the aerogel and its weight. Table 1 is the density calculation data of the

produced aerogels under 2% concentration, which is in accordance with that of cellulose-based chitosan

aerogel [25]. The data showed that, with increase in chitosan level, the aerogel density rose. It implied

that chitosan can shrink the aerogel pores and tighten the MFC/NFC aerogel structure.
 (a)

(a) (b) (c) (d) (e) (f) (g

Figure 1

MFC/NFC aerogel SEM with different chitosan additions. MFC/CH ratio: (a) 100/0, (b) 90/10, (c) 80/20, and (d)

70/30; NFC/CH ratio: (e) 90/10, (f) 80/20, and (g) 70/30.

Table 1

Data on the density of chitosan- (CH-) added MFC/NFC aerogel.

After Ag-NPs loaded, both MFC/CH aerogel and NFC/CH aerogel surface areas were measured after 4 h

degassing at 105°C. The results are listed in Table 2. In Table 2, NFC/CH aerogel has lower BET data

than MFC/CH after Ag loaded. Due oxidation, the NFC possessed the acidic group content up to 400

μmol/g, while MFC possessed the acidic group content of 70 μmol/g. As a result, NFC was more active

with chitosan and formed a tighter aerogel structure [25]. Accordingly, its BET is smaller than that of

MFC/CH aerogel. The higher BET data also imply that the aerogel has more space exposure to which

gives pores benefit particles/solution filling. As a result, we found that the MFC/CH aerogel loaded more

nanoparticles than the NFC/CH aerogel (see Table 3).

Table 2

BET of both MFC/CH aerogel- and NFC/CH aerogel-loaded Ag-NPs.

Table 3

Ag-NP content in MFC/NFC aerogels.

3.2. MFC/NFC Aerogel Microscopy

MFC/NFC aerogels with different chitosan addition levels were conducted and scanned using a SEM.

Generally, chitosan can cause the aerogel dense structure with the increase in addition level (see Figure

1). The structural change is clear also in these SEM images. When MFC aerogel contains 0% chitosan, its

structure is open and the pores are easily seen (Figure 1(a)). When a small amount of chitosan solution

added (Figure 1(b)), we can see the light “films” formed among pores like fogs. With increasing chitosan

content to 20% (Figure 1(c)), these light “films” became thicker. After 30% chitosan added (Figure 1(d)),

these films were so dense that the aerogel structure had less existing pores. This is because of the

characteristic properties of chitosan, natively containing the high content of primary amino groups.

Cellulose with several compounds which having primary amino groups, such as polyethylenimines,

ethylenediamine, and benzyl amine, revealed the formation of new chemical bonds in the materials

processed even at room temperature [20]. Here aerogel making employed the main reaction between

amino and carbonyl groups, besides hydrogen bonds of cellulose and chitosan groups, to improve its

mechanical strength [20, 25]. Since NFC has much more exposed carboxyl/carbonyl groups than MFC,

theoretically NFC/CH aerogel would result in more reaction between NFC and chitosan. In Figure 1, we

did observe the tighter structure of NFC/CH aerogels (pictures E, F, and G in Figure 1) than that of

MFC/CH (pictures A, B, C, and D in Figure 1). Fewer pores but more “films” were formed in NFC/CH

aerogel. The data presented in Tables 1–3 are additional evidences to confirm this observation.

After Ag-NPs loaded, these aerogels exhibited similar SEM morphology to that of Ag-NPs unloaded, in

which structures are denser with the increase in chitosan. This denser structure caused the nanoparticles

to fill differently. Denser aerogel has relatively tight structure and fewer capillaries, which penetrates less

Ag+ and reducing solution, resulting in fewer Ag-NPs generated. Table 3 shows the amount of Ag-NPs in

MFC/NFC aerogels after 575°C oxygen for 25 min isothermal time under TGA. It disclosed that NFC
aerogel has loaded fewer Ag-NPs than MFC aerogels.

In order to investigate how the nanoparticles are located in these aerogels, the MFC/CH and NFC/CH

aerogels with Ag-NPs were scanned by using SEM in high magnification. The images are shown in

Figure 2. Since nanoparticles are expected to locate evenly in smaller size on the composite, any

aggregates should be avoided. All NFC aerogels showed particle aggregates (pictures D, E, and Figure 2),

but only MFC-30% CH aerogel showed Ag-NP aggregates (picture C in Figure 2). The formation of Ag-

NP aggregates may be from the rich hydroxyl and carboxyl groups which absorb much Ag+ solution. But

there are less free hydroxyl and carboxyl groups in denser aerogel after drying. While ‘films’ are formed,

the Ag+ concentrate was forced to sit in pores and then enwrapped as aggregates. These free groups

present negative charge, providing the anchor sites for Ag + uniformly in loose aerogels of MFC/CH with

10% and 20% chitosan. They are better aerogels for nanoparticle loading.

(a)

(a) (b) (c) (d) (e) (f)

Figure 2

Ag-NPs in MFC/CH aerogel: (a) 10%CH, (b) 20%CH, and (c) 30%CH; NFC/CH aerogel: (d) 10%CH, (e) 20%

CH, and (f) 30% CH.

Ag-NP size and distribution for aerogel are very important. Based on good particle distribution in SEM

images shown in Figure 2, MFC aerogel with 20% CH was chosen and TEM observation was conducted

(see Figure 3). From the TEM image, we can see that the particles are monodispersed and have very small

size. Using ImageJ software, the TEM image shown in Figure 3(a) was analyzed for particle size

distribution automatically with every size scale bar (0.72 nm) starting at 4.13 nm. Most particles are in the

range of 4–9 nm with a mean diameter of 7.08 nm. This is because the aerogel was treated by very dilute

AgNO3 solution (10 mM) and there were less Ag + surrounding nanofibrils, typically at negative charged

groups, which are the anchors to be the nucleus of particle growth. Nanofibrils played an important role to

physically stop the Ag + free movement, and then monodispersed small particles were formed. With more

chitosan in aerogels, since chitosan amino groups consumed some carbonyl groups on MFC/NFC, and

most possibly chitosan molecules have strong hydrogen bonds with MFC/NFC (it is to observe “films” in

SEM images), and these aerogels lost many uniform places to accommodate Ag+, resulting in particle

aggregates, as we can see in C, D, E, and F of Figure 2.

(a)

(a) (b)

Figure 3

TEM images of MFC/CH aerogel-loaded Ag-NPs. 20% CH (a) and particle size range (b).

3.3. FTIR Spectroscopy

The spectra of MFC aerogel with 20% chitosan is shown in Figure 4, along with MFC aerogel blank and
−1
NFC/CH areogel (marked as B, A, and C respectively, in Figure 4). The peaks at 3330–3340 cm

corresponded to the stretching vibration of hydroxyl groups. These peak intensities reinforced for

MFC/NFC aerogel blended chitosan due to the N–H groups involvment [39]. The main change observed
−1 −1
in the spectra is no sharp peaks at 1650 cm which corresponded to the carbonyl stretch and 1560 cm

to the amino groups of chitosan in B and C of Figure 4, implying the chemical reaction between chitosan

and cellulose [20]. This also explained why we observed the aerogel tight structure with chitosan under

SEM.

Figure 4

MFC/NFC aerogel FTIR spectra with chitosan 20%. Note: A, MFC aerogel 0% CH; B, MFC aerogel 20% CH; C,

NFC aerogel 20% CH.

3.4. Thermal Gravimetric Analysis (TGA)

In view of the importance of thermal stability in many applications of MFC/NFC aerogels, we examined

thermal decomposition of composite-loaded Ag-NPs by thermogravimetry (TGA, Perkin Elmer Q500,

and heating rate of 10°C/min) in a nitrogen atmosphere under 500°C, as shown in Figure 5. In all TGA

curves, the small weight losses below 150°C apparently resulted from evaporation of adsorbed moisture.

Under nitrogen, the decomposition behavior of the MFC-Ag aerogel was nearly the same with different

levels of chitosan, the most weight loss taking place at 280°C; meanwhile, NFC-Ag aerogels have lower

decomposition temperature of around 250°C. Chitosan did not change both MFC and NFC aerogel

thermal stability. In order to obtain the Ag-NP amount in aerogel, TGA under oxygen in the range of 500–

575°C was continued. The isothermal time for 25 min at 575°C was set up. The results are listed in Table

3. The Ag-NPs in MFC/CH aerogel has slightly higher amount than that in NFC/CH aerogel, but the

former has more uniform particle distribution.

(a)

(a) (b)

Figure 5

TGA behavior of MFC-Ag aerogels with different chitosan addition and NFC-Ag aerogels with different chitosan

addition. Note: TGA under N2 atmosphere till 500°C and then switched to oxygen to 575°C.

3.5. Antibacterial Activity Testing

The antibacterial activity of these four samples MFC80/CH20, NFC80/CH20, MFC80/CH20/Ag-NPs,

and NFC80/CH20/Ag-NPs was tested against E. coli by using the viable cell-counting method. NFC

aerogel without chitosan was compared. The effects of aerogels on the growth of the recombinant bacteria

E. coli are shown in Figure 6. “Blank” in Figure 6 means a plate which was produced from untreated

bacterial solution. As shown in the plates, no bacterial colonies were observed at concentrations of 7 ×

107 CFU/mL for both MFC/CH-Ag-NPs and NFC/CH-Ag-NPs which represent the highest antibacterial

activity. On the other hand, many bacterial colonies were observed for MFC-CH, NFC-CH, and NFC

aerogels which implied poor antibacterial activity. Though chitosan is considered as a good natural

polymer for medical application due to its antibacterial property, Ag-NPs in these aerogels imported much

better inhibition of bacteria than chitosan. MFC/CH-Ag-NPs may have better antibacterial property than

NFC/CH-Ag-NPs since the former has excellent nanoparticle distribution. This should be further

examined.
 Figure 6

Antibacterial activity of NFC, MFC/chitosan, NFC/chitosan, MFC/chitosan/Ag-NPs, and NFC/chitosan/Ag-NPs

against E. coli.

4. Conclusions
In the current work, we successfully utilized chitosan as MFC/NFC aerogel reinforcement biopolymer.

The reinforced aerogels have overcome the water unstability. With more chitosan addition, MFC/NFC

aerogels became denser which have tighter structures that are observed in SEM. Chemical reaction

occured between chitosan and MFC/NFC. Comparing both MFC/CH and NFC/CH aerogels, MFC/CH

aerogel has higher BET surface area and lower density than NFC/CH aerogel. Ag-NPs were in site loaded

to chitosan-added MFC/NFC aerogel. The MFC/CH aerogel performed much better than the NFC/CH

aerogel, which obtained monodispersed nanoparticles of Ag-NPs. Finally, both MFC/CH-Ag-NP and

NFC/CH-Ag-NP aerogels exhibited excellent antibacterial activity. But the better antibacterial

performance of both aerogels should be further examined.

Data Availability
The data used to support the findings of this study are available from the corresponding author upon

request.

Conflicts of Interest
The authors declare no conflicts of interest.

Acknowledgments
The authors would like to thank Prof. Orlando J. Rojas and his group for their help during this research

and in editing the manuscript. The Special Support Plan for Xijiang Innovation Team Plan 2016, High-

Level Talent Cultivation of Guangdong Industry Polytechnic (No. KYRC2018-020), and Guangdong

University Youth Innovation Fund Project (No. 2018GKQNCX032) are greatly acknowledged for the

support.

Supplementary Materials
The SEM images showing the surface of MFC aerogel with 10% chitosan addition and 20% chitosan

addition. (Supplementary Materials)

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Copyright
Copyright © 2020 Huanlei Yang et al. This is an open access article distributed under the Creative

Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any

medium, provided the original work is properly cited.

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