Materials Science & Engineering C 98 (2019) 1277–1293

Contents lists available at ScienceDirect

Materials Science & Engineering C

journal homepage: www.elsevier.com/locate/msec

Review

Bacterial cellulose nanocomposites: An all-nano type of material T

⁎
F.G. Torres , J.J. Arroyo, O.P. Troncoso
Department of Mechanical Engineering, Pontificia Universidad Católica del Perú (Lima 32 Perú), Av. Universitaria 1801, Lima 32, Lima, Peru

A R T I C LE I N FO A B S T R A C T

Keywords: Bacterial cellulose (BC) is a fascinating polymer with a three-dimensional structure formed by nanofibers of pure
Bacterial cellulose cellulose, synthesized by some bacteria and organized as a coherent network. Its biocompatibility and re-
All-nano composites markable mechanical properties have promoted scientific interest for its use in a variety of applications including
Undisturbed bacterial cellulose network biomedical, electrical, among others. However, it is the possibility of incorporating nanosized materials into the
Bacterial cellulose applications
coherent 3-D network structure displayed by BC what has propelled multiple investigations on the development
of BC nanocomposites for different applications. Here we report the different methods and techniques used so far
for the BC nanocomposites production. We have focused on the processing techniques that allow the in-
corporation of functional nanoreinforcements, nanofillers and additional phases without disturbing the original
network structure, leading to the formation of nanomaterials. Processing methods, resulting structure-property
relationships and potential applications of these novel nanocomposites are discussed and showcased as a fair
example of integrated design and manufacture of materials.

1. Introduction linear β-1,4-glucan chains and produce an extracellular secretion of the

formed chains. Last, they assemble and crystallize the chains into
Manufacturing companies, government agencies at all levels and composed ribbons. This process leads to the formation of a coherent
consumers increasingly require the use of biodegradable materials, in ultra-thin three-dimensional network of cellulose nanofibers aligned in
order to reduce the environmental impact generated by the current parallel to the surface of a liquid medium (see Fig. 1). This network is
lifestyle. Natural cellulose-based materials (which are the most abun- called a pellicle and its geometry is determined by intra- and inter-
dant polysaccharides in nature [1–3] and include wood, hemp, cotton, molecular hydrogen-bonding network, hydrophobic and van der Waals
among others) have been used for a long time by our society for these interactions [11].
applications due to their wide availability, renewability, and biode- BC has a crystallographic structure typical of cellulose type Iα [12],
gradability. Along the same lines, the study and use of bacterial cellu- with a degree of crystallinity up to 90% [13]. The several hydroxyl
lose is relatively recent. Despite sharing a common backbone, there are groups on BC surface make it a hydrophilic material [14]. BC nanofi-
marked differences between plant and bacterial cellulose. Plant fibers bers are around 20–100 nm in diameter and display a surface area su-
are composed of lignin, hemicelluloses, pectin and only 40–70% of perior to that of vegetal cellulose [15]. Grande et al. [16] analyzed the
cellulose [4]; in contrast, bacterial cellulose is made up of pure cellulose mechanical properties of BC films, yielding an average tensile strength
nanofibers, displaying high purity and strength, without requiring of 241.42 ± 21.86 MPa, a maximum elongation value of
subsequent refining treatments. Owing to these unique characteristics, 8.21 ± 3.01% and Young's modulus of 6.86 ± 0.32 GPa.
bacterial cellulose (BC) has been extensively studied and characterized The functionality, flexibility and excellent mechanical properties of
[5–8]. bacterial cellulose have been considered adequate for certain applica-
BC is a material synthesized extracellularly by certain types of tions in the past. However, the contemporary need for BC-based pro-
bacteria such as Acetobacter, Azotobacter, Gluconacetobacter, ducts with superior properties to meet the demand in diverse fields
Pseudomonas, Salmonella and Sarcina ventriculi [6]. Among them, the becomes increasingly evident. Modern BC-based composites involve the
most effective and, thus, the most used bacteria for cellulose production use of nanosized elements of particular characteristics. Since BC has a
are Gluconacetobacter xylinum, Gluconacetobacter hansenii, and Gluco- nanofibers arrangement, the developed materials consist of the inter-
nacetobacter pasteurianus [9]. According to Czaja et al. [10], cellulose action of two nanometric structures, which we call nano-nano compo-
biosynthesis starts when bacteria polymerize glucose residues into sites.

⁎
Corresponding author.
E-mail addresses: fgtorres@pucp.pe (F.G. Torres), junior.arroyo@pucp.edu.pe (J.J. Arroyo), troncoso.op@pucp.pe (O.P. Troncoso).

https://doi.org/10.1016/j.msec.2019.01.064
Received 10 May 2018; Received in revised form 14 January 2019; Accepted 14 January 2019
Available online 16 January 2019
0928-4931/ © 2019 Elsevier B.V. All rights reserved.
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 1. Hierarchical structure of bacterial cellulose. The bacteria of the genus Acetobacter produces a three-dimensional BC network composed of fibrils. In turn, each
BC fibril is composed of a bunch of BC microfibrils. Each BC microfibril is made of several nanofibrils.

Here we review a variety of studies regarding the processing tech- were improved by 128.8% and 1110%, respectively. Phomrak et al.
niques that allow the incorporation of functional nanoreinforcements, [35] developed natural rubber composites reinforced with BC via a
nanofillers, and additional phases into bacterial cellulose, with a par- latex aqueous microdispersion process. The hydrophilicity, opacity, and
ticular interest on those produced without disturbing the original BC crystallinity of the composite were improved by incremental BC
network structure. The nanomaterials used for the preparation of BC- loading. The reinforcement with BC nanofibers yields a material with
based nanocomposites are reviewed, including conducting polymers 4128.4 MPa of Young's modulus and tensile strength of 75.1 MPa. At
[17,18], graphene oxide [19,20], carbon nanotubes [21], ceramics lower BC nanofibers reinforcement, the material presented high elastic
[22,23] and biopolymers [24,25]. We also explain how the addition of elongation, which may be suitable for rubber-based products and elastic
these nanomaterials improve the electrical, optical and mechanical packaging.
properties of BC, enabling its application in acoustic diaphragms [26],
supercapacitors and biosensors [27], and biomedical applications
[28–30]. A systematic classification of the BC-based materials is pro- 2.2. Conductive polymers
posed, taking into account i) the BC fiber network final state (destroyed
or preserved), and ii) the technique used to incorporate the second The discovery of the high conductivity of polyacetylene [36] opened
phase. a highly explored path of conductive polymers. These are a family of
highly conjugated polymers with spatially extended π-bonding, which
present unique electrical, electrochemical and optical properties [37].
2. Materials used for the preparation of bacterial cellulose
The aim of incorporating conductive polymers into BC is to develop
nanocomposites
flexible nanocomposites that can be used as electrolytes or stimuli-re-
sponsive membranes in solar energy devices, biosensors and biomedical
It is indeed the ability to incorporate other materials into the co-
devices. Among the most used conductive polymers are polyaniline
herent BC network structure what has allowed for the development of a
(PAni), polypyrrole (PPY), poly(3,4-ethylene dioxythiophene) (PEDOT)
variety of nanocomposites for multiple applications. In this section, we
and poly(p-phenylene vinylene) (PPV).
review the different types of materials that have been used so far in BC
nanocomposites formation.

2.2.1. Polyaniline
2.1. BC nanofibrils as reinforcing fillers Polyaniline belongs to the semi-flexible rod polymer family, which
are organic polymers transformed into conductive polymers through
Bacterial cellulose can be used as a reinforcement of nanoscale di- oxidation or doping mechanisms [38]. Wang et al. [39] developed BC-
mensions, whereas the micrometer-scale diameter of polymer fibers can supported polyaniline by in situ polymerization of aniline onto the BC
act as a substrate for BC attachment. Juntaro et al. [31] developed a matrix. The nanocomposite displayed an electrical conductivity of
process to cover sisal fibers with BC. They used these BC-covered sisal 5.1 S cm−1 and a mass capacitance of 273 F·g−1 at 0.2 A·g−1. Marins
fibers to reinforce a poly-L-lactic acid (PLA) matrix. First, they added et al. [40] added polyaniline doped with dodecylbenzene sulfonic acid
the sisal fibers (tensile strength and Young's modulus of 383 MPa and by in situ chemical polymerization on hydrated BC sheets, which led to
15.2 GPa, respectively) to the BC growth medium. After 4–7 days of a conductivity of 2.09 × 10−2 S cm−1. Müller et al. [18] followed a
incubation a transparent BC pellicle covered the sisal fibers. The fiber similar procedure, adding polyaniline through in situ oxidative che-
pull-out tests showed that the interfacial adhesion of the BC-covered mical polymerization of BC films, with FeCl3·6H2O as oxidant and the
sisal fibers was increased. The elastic modulus and tensile strength of presence of HCl in an aqueous solution. They reported a conductivity of
the BC/PLA composites was higher when the BC-covered sisal fibers 0.9 S cm−1, evidencing that the crystalline structure of BC remained
were used (11.21 GPa and 113.8 MPa, respectively, in contrast to intact and the electrical properties improved as the reaction time in-
7.91 GPa and 78.9 MPa). Pommet et al. [32] used a similar procedure to creased since it stimulated a more significant and complete coating.
incorporate bacterial cellulose-modified sisal fibers into cellulose Likewise, Hu et al. [17] performed an in situ oxidative polymerization
acetate butyrate matrices, reporting a significant improvement of in- of PAni, improving the thermal stability and finding a conductivity of
terfacial adhesion and mechanical performance. Lee et al. [33] used 5 × 10−2 S cm−1 for a PAni content of 10.7 wt% and a reaction time of
acrylated epoxidised soybean oil (AESO) to develop sisal fiber/poly- 90 min. Moreover, the mechanical measurements gave a Young's
AESO and BC-sisal fiber/polyAESO composites. The tensile modulus for modulus value of 5.6 GPa and a tensile strength of 95.7 MPa, being
neat polyAESO was 0.4 GPa. The addition of 40 vol% sisal fibers im- superior to pristine BC characteristics. Recently, Wan et al. [41] de-
proved the tensile modulus to 3.2 GPa, and further improvement was veloped a flexible BC/graphene/PAni by uniform dispersion of gra-
achieved with BC used as a binder, up to 5.6 GPa. Bacterial cellulose phene on the BC matrix and a subsequent PAni deposition on the sur-
nanofibers were used as a filler for glass-fiber-reinforced epoxy com- faces of graphene layers and BC fibers. They reported an electrical
posites [34]. By the incorporation of 0.3 wt% BC nanofibers, the inter- conductivity of 1.7 S cm−1.
laminar fracture toughness for crack initiation and crack separation

1278
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

2.2.2. Polypyrrole be associated with the hydrophilic bacterial cellulose matrix, occupying
Polypyrrole is another organic polymer formed by the polymeriza- its void spaces and interacting with BC fiber chains [37]. Due to their
tion of pyrrole. PPy and its derivatives exhibit excellent properties, such size and the surface effects, they allow adjusting the properties of the
as good environmental stability, electrical conductivity, high energy final nanocomposite. Some of the metal nanoparticles used in the past
density, and ease to synthesize [42]. Li et al. [43] formed highly con- for BC nanocomposites include iron, silver, gold, copper, palladium and
ductive paper electrodes using bacterial cellulose–polypyrrole nanofi- metal alloys, among others.
bers filled with multi-walled carbon nanotubes. The paper electrodes Zhang et al. [55] used magnetite (Fe3O4) nanoparticles to reinforce
presented a stable and efficient performance, with a capacitance of BC through in situ synthesis of Fe3O4, developing a flexible magnetic
2.43 F cm−2. Similarly, Peng et al. [44] deposited polypyrrole and membrane. They achieved a homogeneous distribution of magnetite
nickel sulfide on BC fibrous membranes, reporting a conductivity of over the matrix. Zhu et al. [56] employed Fe3O4 as an adsorbent for
5.1 S cm−1, a specific capacitance of 713 F·g−1 and an energy density of heavy metal ions, reporting a high adsorption capacity and recyclability
239 Wh kg−1 at a current density from 0.2 to 1.6 mA cm−2. Müller et al. after ions elution. Sriplai et al. [57] fabricated magnetic BC composites
[45] performed an in situ polymerization of pyrrole (Py) in a BC film by immersing a freeze-dried scaffold into a water-based ferrofluid
using ammonium persulfate (APS) and FeCl3·6H2O as oxidants. BC/PPy- containing Fe3O4 magnetic nanoparticles. Their sensitivity to external
APS presented homogeneously distributed spherical conductive nano- magnetic forces opens a nearly exhaustless potential of possible appli-
particles, while BC/PPy-FeCl3 revealed the formation of a continuous cations.
conductive layer that covered BC nanofibers. After analyzing the me- Silver and its derivatives exhibit strong inhibitory and bactericidal
chanical and electrical properties of the BC/PPy nanocomposites, they effects [58–60] and have been used for many biomedical applications
reported a conductivity of 2.7 S cm−1 and tensile strength of 4.1 MPa [61,62]. Maneerung et al. [58] immersed a BC film into a silver nitrate
when FeCl3·6H2O was the oxidant agent. Lay et al. [42] performed the solution. Then, sodium borohydride was used to reduce the in-
in situ polymerization of pyrrole on BC, using FeCl3. The BC/PPy corporated Ag+ into metallic silver nanoparticles. The results showed
membrane acquired a conductivity of 3.9 S cm−1 and a specific capa- strong antimicrobial activity of the BC/silver films against Escherichia
citance of 191 F·g−1, which could be fully implemented in biomedical coli and Staphylococcus aureus. Wu et al. [63] developed a novel method
sensors and energy storage devices. to perform an in-situ synthesis of Ag nanoparticles on BC membranes.
BC membranes were soaked in a silver ammonia solution (Tollen's re-
2.2.3. PEDOT agent). The guest molecules of Tollens' reagent diffused into the inner
Developed by the Bayer AG® research laboratories in Germany [46], spaces of BC nanopores and reacted with cellulose fibers, forming an
poly(3,4-ethylene dioxythiophene) or simply known as PEDOT is an AgNP-BC composite. The results showed a strong interaction between
insoluble polymer, with interesting characteristics such as high con- the silver nanoparticles and BC fibers, which prevented the drop of Ag
ductivity, transparency in thin and oxidized films, and high stability in nanoparticles from the BC network, minimizing toxic effects. AgNP-BC
the oxidized state [47]. In order to make PEDOT processable, poly exhibited significant antibacterial activities with more than 99% re-
(styrene sulfonic acid) is used as dopant. PSS reduces the conductivity ductions in Escherichia coli, Staphylococcus aureus and Pseudomonas
of PEDOT from 300 S cm−1 to 10 S cm−1, but PEDOT:PSS samples aeruginosa.
display high visible light transmissivity and great stability [48]. Khan Gold nanoparticles receive the attention of researchers due to their
et al. [49] carried out the ex situ incorporation of commercial poly(3,4- outstanding optical, electronic, and chemical properties [64]. BC/Au
ethylene dioxythiophene)-poly(styrene sulfonate) (PEDOT:PSS) nanocomposites have been used as catalyst [65–67], trace concentra-
polymer into BC pellicles. The BC/PEDOT:PSS nanocomposites dis- tion detection [68] and biosensors devices [69]. Zhang et al. [69] re-
played a conductivity of 12.17 S cm−1, which is one of the highest duced HAuCl4 with polyethyleneimine (PEI, a reducing agent) in a
values obtained for BC-based nanocomposites. Kim et al. [50] deposited solution to obtain Au nanoparticles in aqueous dispersion. The authors
PEDOT:PSS conductive layers on the top and bottom of a BC film by uniformly coated BC nanofibers using the nanoparticle suspension,
dipping and drying it, forming electro-active hybrid actuators. Aleshin considering the PEI role as a linking agent. Subsequently, a biosensor
et al. [51] synthesized BC/PEDOT:PSS, which presented a strong ab- was developed by embedding horseradish peroxidase (HRP) in the
sorption near the infrared spectral region, with a potential application structure of the BC/Au nanocomposite, which displayed a high sensi-
in the development of biocompatible electrodes. Bu et al. [52] evenly tivity detection of H2O2. Liu et al. [70] elaborated conductive cellulose
coated the surface of BC fibers with PEDOT, forming an ultrathin films by a self-assembly procedure, using an aqueous gold dispersion of
flexible paper electrode, which displayed a volumetric capacitance of nanoparticles. The films displayed an electrical conductive behavior
106.3 F cm−3 at a volumetric current density of 0.83 A cm−3. when the gold nanoparticle loading was higher than 20 wt%.
Peng et al. [71] used BC covered with polypyrrole/copper oxide to
2.2.4. Polyphenylene vinylene prepare a conductive membrane. The BC/polypyrrole/copper oxide
The first polymer light-emitting device was based on poly(p-phe- membrane had an electrical conductivity of 7.4 S cm−1 and a capaci-
nylene vinylene) or also named polyphenylene vinylene [53], which is tance of 601 F·g−1, being suitable for flexible energy-storage devices.
a highly stable conjugated polymer. Aleshin et al. [54] built up a Among other nanoparticles, Chen et al. [72] synthesized zinc oxide
flexible light-emitting transparent paper based on bacterial cellulose. particles using a polyol method, to introduce Zn2+ ions. Peng et al. [44]
They saturated a BC film with MEH-PPV (poly[2-methoxy-5-(2-ethyl- coated the BC membrane with polypyrrole/nickel sulfide, achieving a
hexyloxy)-1,4-phenylene]vinylene) by dipping the BC film in a MEH- conductivity of 5.1 S cm−1. Yang et al. [73] carried out the in situ de-
PPV/chloroform solution for 15 h. The photo-luminescence spectro- position of Pt nanoparticles on BC, finding that the BC/Pt membrane
scopy tests showed that the photoluminescence spectrum of BC/ presented a high electrocatalytic activity in the hydrogen oxidation
MEH:PPV films contained emission contributions from both BC and reaction.
MEH:PPV. This result suggests that BC/MEH:PPV nanocomposites BC films were immersed in a mixture solution of PdCl2 and CuCl2 in
could be used for the production of transparent light-emitting papers water. The adsorbed metallic ions were reduced inside the BC matrix to
for display, lighting and biosensor devices. Pd-Cu nanoparticles using potassium borohydride, obtaining a compo-
site with high catalytic activity [74]. Olsson et al. [75] developed a stiff
2.3. Metals magnetic nanopaper using bacterial cellulose fibrils as templates for
ferromagnetic cobalt ferrite nanoparticles growth.
A different approach to enhance the properties of BC nanocompo-
sites is the use of metallic nanoparticles. These inorganic materials can

1279
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 2. Addition of carbon nanotubes to the BC structure monitored through FE-SEM images. (a) Vacuum-dried bacterial cellulose membrane, (b) Purified MWCNTs
and (c) MWCNTs incorporated into the bacterial cellulose membrane.
Extracted from Yoon et al. [97].

2.4. Graphene and derivatives membrane. Once the medium was consumed, the procedure was re-
peated, until the desired thickness was reached. The developed hy-
Several studies have reported the incorporation of two-dimensional drogels presented improved mechanical properties in comparison with
reinforcements such as graphene, graphene oxide, reduced graphene BC and previously reported BC/GO composites.
oxide and carbon nanotubes [76–81] in BC, with the aim of improving Graphene oxide has also been used in its reduced form. The reduced
the mechanical and electrical properties of pristine BC matrix. graphene oxide (RGO) formation can be carried out thermally [89,90],
chemically [90–92] or by irradiation [93,94], enhancing the con-
2.4.1. Graphene ductivity and partially recovering the original structure and properties
Graphene, the first two-dimensional atomic crystal available, pre- of graphene [85]. Nandgaonkar et al. [95] prepared BC/RGO using a
sents outstanding mechanical stiffness, strength, high thermal and culture medium that allows synthesizing the fibers during their com-
electrical conductivity [82], and a large specific surface area. The use of bination with RGO, reporting a conductivity of 2.37 × 10−1 S cm−1.
graphene and its derivatives could impressively enhance the inherent Recently, Ccorahua et al. [20] also developed BC/RGO nanocomposites
properties of BC. Luo et al. [79] dispersed graphene in the BC culture using an in situ hydrazine treatment, obtaining a conductivity of
medium using a layer-by-layer interface culture strategy to obtain BC/ 12 × 10−2 S cm−1.
graphene nanocomposite hydrogels. The methodology consists of re-
petitive cycles of spraying the culture medium onto the base membrane 2.4.3. Carbon nanotubes
until it is completely consumed. The BC/graphene hydrogels exhibited Carbon nanotubes are allotropes of carbon, formed by graphene
91% improvement in tensile strength and 279% improvement in tensile sheets wrapped in a nano-cylindrical tube. The addition of small
modulus compared to pure BC. Zhou et al. [83] added graphite nano- amounts of carbon nanotubes to BC contributes to the improvement of
plates to pristine BC membranes using two methods: immersion and the mechanical strength, electrical conductivity, and thermal con-
sonication. The comparison showed a more significant increase in ductivity [96]. Yoon et al. [97] prepared BC/multi-walled carbon na-
electrical conductivity for sonication (conductivity of 1.2 S cm−1). Shao notubes (MWCNTs) nanocomposites (Fig. 2). They used sodium dode-
et al. [84] crushed BC pellicles using a high speed homogenizer to cylbenzene sulfonate to disperse MWNTs in water and then immerse the
achieve BC fiber slurry. Graphene aqueous solution was added into the BC film in the resulting solution. The reported conductivity was
BC homogenate and treated by ultrasonication followed by preparation 4.2 × 10−1 S cm−1. Li et al. [98] incorporated MWCNT's and polyani-
of BC/graphene composite films. Results showed that graphene addi- line in a BC membrane to prepare flexible electrodes for flexible su-
tion decreased the water retention capacity of BC, although the me- percapacitors. The BC/MWCNT/PAni electrodes had an excellent spe-
chanical properties were enhanced in comparison to pure BC. These cific capacitance (656 F·g−1 at a discharge current density of 1 A·g−1)
results are attributed to a uniform dispersion of graphene in the BC and remarkable cycling stability with capacitance degradation less than
matrix, good miscibility and strong interfacial interactions between 0.5% after 1000 charge-discharge cycles (at a current density of
them [78]. 10 A·g−1).

2.4.2. Graphene oxide 2.5. Ceramic

Graphene is a relatively new material with extraordinary mechan-
ical and electrical properties. Graphene oxide (GO) in turn exhibits a Certain mineral elements such as hydroxyapatite, silica, and cal-
high hydrophilic behavior, which enhances the formation of stable cium carbonate have been investigated for biomedical applications, due
aqueous colloids and the assembly of macroscopic structures [85]. Feng to their biocompatible, non-toxic and hard tissue-mimicking nature.
et al. [76] developed BC/GO nanocomposites using an immersion Ceramic nanoclays stand out for their mechanical reinforcing cap-
technique, achieving a conductivity of 3.5 × 10−2 S cm−1. Shao et al. ability.
[86] synthesized BC/GO by a sonochemical method. After its char-
acterization against Escherichia coli and Staphylococcus aureus, they 2.5.1. Hydroxyapatite
concluded that the composite presented excellent antibacterial activ- Hydroxyapatite (HAp) is a phosphate mineral formed by calcium
ities. Liu et al. [87] developed a hybrid composite based on the che- phosphate, commonly used in bone grafting [99,100], and bone drug
mical bonding of bacterial cellulose and graphene oxide coated with delivery [101], which displays a structure and chemical composition
polypyrrole. The resultant material presented high electrical con- similar to those of bone minerals. Grande et al. [23] prepared BC/HAp
ductivity (1.32 S cm−1) and large volumetric capacitance (278 F cm−3). nanocomposites by introducing HAp in the culture medium. The re-
Luo et al. [88] used a layer-by-layer assembly strategy. A pure BC sulting nanocomposites were found to be adequate for biomedical ap-
membrane was used as a base (named BC0). They added a GO sus- plications. Fig. 3(a) presents a schematic representation of the inclusion
pension to the culture medium of BC, and the GO-dispersed culture of HAp nanoparticles within the BC matrix. Fig. 3(b) shows the dis-
medium was sprayed on the surface of BC0, building a BC/GO tribution of those nanoparticles in the BC 3-D network. Wan et al. [102]

1280
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 3. Incorporation of nanosized fillers in the BC nanonetwork. (a) Schematic representation of the incorporation of nanoparticles in the BC scaffold. (b) SEM image
of the incorporation of hydroxyapatite in the BC matrix. 4(b) was extracted from Grande et al. [23].

phosphorylated BC for enhancing its capability to induce HAp forma- montmorillonite at different concentrations in a BC matrix. They as-
tion. The results revealed that phosphorylation effectively triggered sessed the antibacterial activities of BC-based films against Escherichia
HAp formation compared with unphosphorylated BC. Zimmermann coli and Staphylococcus aureus, showing an excellent response at a high
et al. [103] negatively charged BC with the adsorption of carbox- montmorillonite concentration.
ymethyl cellulose (CMC) to initiate the nucleation of calcium-deficient
hydroxyapatite (cdHAp). Saska et al. [104] developed nanocomposites 2.6. Biopolymers
by using BC membranes incubated in solutions of CaCl2 followed by
Na2HPO4. The nanocomposites were effective for bone defect re- 2.6.1. Collagen
generation in rat tibiae. Hutchens et al. [105] deposited cdHAp in a Collagen is a natural biopolymer that forms fibers in several animal
bacterial cellulose hydrogel in order to prepare a composite mimicking tissues and organs. Despite its huge flexibility, collagen displays a high
the natural biomineralization of bone. tensile strength, which has motivated its application in the biomedical
field. Zhijiang and Guang [121] immersed BC in a solution of collagen
2.5.2. Silica in acetic acid and then filtered the collagen excess. After filtration, the
Silica is the major component of sand, obtained by sand mining and material was freeze-dried. The crystalline structure remained un-
purification of quartz. Yano et al. [106] prepared nanocomposites of BC changed, although the thermal stability improved. Besides, Young's
filled with silica (SiO2) following two methods: silica addition to the modulus and tensile strength increased, which makes the composite
culture medium and BC hydrogels immersion. Maeda et al. [107] de- suitable for wound dressing. Saska et al. [122] modified BC by glycine
veloped a BC/silica hybrid through immersion and posterior hot esterification in order to crosslink it with type I collagen. The nano-
pressing, obtaining an improved Young's modulus and tensile strength composite possessed a more flexible structure, which makes it easy to
of 17 GPa and 185 MPa, respectively. BC/silica nanocomposites have handle during surgical procedures. Luo et al. [123] prepared BC/col-
been proposed as aerogels [108], light emitting silicon-based materials lagen nanocomposites by adding collagen to the BC culture medium. BC
[109] and adsorbents for water purification [110]. reduced its porosity and roughness after collagen incorporation. The
results showed changes in the crystallinity, color, and thickness of the
2.5.3. Calcium carbonate BC/collagen films in comparison to pure BC.
Calcium carbonate (CaCO3) is frequently found in rocks as calcite
and aragonite minerals. It is also found in mineralized tissues of bio- 2.6.2. Chitosan
logical systems [111]. Besides the use of BC as a template for HAp Chitosan presents interesting properties such as exudes absorption,
addition, CaCO3 can be placed inside a BC matrix pores [112–114]. antimicrobial and wound-healing characteristics. Ul-Islam et al. [124]
Stoica-Guzun et al. [111] investigated the effect of sonication of CaCO3 immersed BC sheets in a 1% acetic acid solution in which 1% of chit-
on a BC membrane, using CaCl2 and Na2CO3 as reactants. They found osan was dissolved, monitoring the chitosan adsorption at various
that ultrasound irradiation originated bigger crystals with a large temperatures and treatment time. They reported an enhancement of
variety of shapes in comparison to crystals of non-irradiated samples. mechanical properties, water holding capacity and water release rate at
Later, Stoica-Guzun et al. [115] tested the effect of microwave irra- 50 °C in a shaking operation mode, which may lead to its use in bio-
diation, using the same reactants as in their previous work. The results medical applications. Phisalaphong et al. [125] added low-molecular-
showed notorious differences between morphology and polymorphism weight chitosan into the BC culture medium. The BC/chitosan nano-
of irradiated calcium carbonate crystals, with presumably medical and composite prepared had smaller pores compared to pristine BC showing
industrial applications. high mechanical properties in the wet and dry state, high water ab-
sorption capacity and high average surface area. Cai et al. [126] im-
2.5.4. Nanoclays mersed a BC wet pellicle in a solution of chitosan in acetic acid. The
Some studies have shown that the dispersion of nanoclays in a chitosan molecules penetrated the BC structure, forming a multi-layer
polymeric matrix improves its mechanical and barrier properties, its network with great thermal stability (thermal degradation temperature
thermal stability and biodegradability [116–119], which are dependent changed from 263 °C to 366 °C when chitosan content increased from
on the interaction between the matrix and the nanoclays. Perotti et al. 1.2% to 4.5%) and reduced tensile strength and Young's modulus. A
[120] developed BC/laponite clay nanocomposites at different ratios by similar procedure was followed by Kim et al. [127]. They developed
coating a BC film with a dispersion of clay particles in water. They BC/chitosan nanocomposites via BC immersion in a chitosan solution
obtained a significant degree of adhesion that improved the Young's followed by a freeze-drying step. The incorporation of chitosan in the
modulus and tensile strength. Ul-Islam et al. [22] incorporated BC matrix results in a decrease in the degree of crystalline of BC and an

1281
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 4. Schematic representation of the BC/starch formation. (a) Starch granules are in the suspension. (b) Starch is partially gelatinized. (c) BC is synthesized in a
medium with partially gelatinized starch. (d) Formation of the final composite.
Extracted from Grande et al. [24].

improvement in thermal stability and biocompatibility with almost molecules, it has a nanofibers arrangement. Therefore, it can be con-
unchanged mechanical properties. Lin et al. [128] also produced BC/ sidered as a supra-molecular structure of nanometric dimensions. Since
chitosan nanocomposites by immersing BC films into a chitosan solu- most of the dispersed phases also present a nanometric scale size, the
tion. They reported that the BC/chitosan nanocomposites prepared re- majority of BC nanocomposites are formed from the interaction of two
tain moisture in time without dehydration and inhibit bacterial growth. nanometric supra-molecular structures. In that sense, considering the
They used the BC/nanocomposites as wound dressings and found faster components that lead to the formation of BC nanocomposites (see
wound regeneration in comparison to pure BC dressings. classification diagram in Fig. 5), the generated material should be
adequately denominated a nano-nano composite.
2.6.3. Gelatin and starch
Other biopolymers that interact with BC for the development of 3. Processing methods used for the production of bacterial
nanocomposites are gelatin and starch. Nakayama et al. [129] synthe- cellulose nanocomposites
sized BC/gelatin by immersing a BC film in an aqueous solution of
gelatin. Despite the poor mechanical characteristics of gelatin, BC/ge- Numerous methods have been developed to produce nano-nano
latin double network gels can sustain almost 3 MPa and display an composites based on BC, with the aim of achieving a correct dispersion
elastic modulus of 23 MPa, 112 times higher than the elastic modulus of of the nanofillers in the BC matrix, avoiding the formation of large
gelatin. Grande et al. [24] developed a self-assembling procedure to aggregates. The use of a particular method depends on the nature of the
incorporate starch into a BC matrix (Fig. 4). They added starch to the combining phase and the envisaged application for the BC nano-
growth medium and autoclaved it, which induced the gelatinization of composites. In general, BC has been used as a matrix (to be loaded with
starch. The bacteria synthesized BC fibers in the presence of the par- nanofillers), or as a reinforcement. Thus, the classification we propose
tially gelatinized starch granules. With this bottom-up process, starch is based on the final state of the BC structure once the nano-nano
was incorporated into the BC network maintaining the crystallinity
degree of native BC with a smooth decrease in the mechanical prop-
erties. Wan et al. [130] incorporated plasticized starch to BC nanofi-
bers. Starch and glycerin were mixed (30% w/w glycerin to starch), and
later the BC membrane was immersed in the solution. The BC/starch
nanocomposite displayed a superior tensile strength and modulus than
starch, but a lower elongation at break.

2.7. Nano-nano structures

The supra-molecular (“all-nano”) architecture of bacterial cellulose,

characterized by its loose fibril arrangement, high aspect ratio, high
surface area per unit mass [131] and a reactive surface due to OH side
groups, provides BC with a tendency to form intra- and intermolecular
bonding [132] (hydrogen bonds or van der Waals forces) and grafting
of chemical species to achieve surface functionalization. This behavior
favored the development of BC nanocomposites through self-assembly
[24], matrix irradiation [133], controlled dispersions within matrix
polymers and controlled particle-matrix bond strength [134].
As emphasized throughout this section, the main characteristic of Fig. 5. Types of nanofillers used with bacterial cellulose for the elaboration of
the BC matrix is that, instead of being a concentrated structure of nano-nano materials.

1282
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 6. Disturbed network methods that lead to the destruction of the original nanonetwork structure of BC.

composite is obtained: i) disturbed or ii) undisturbed network, as illu- nanocomposite films. The nanocomposite films were cut into pieces,
strated in Figs. 6 and 7. stacked into layers of 25 sheets and hot-pressed. The Young's modulus
of the nanocomposites was 28 GPa, higher than the modulus of pure BC
3.1. Disturbed network sheets (19 GPa). They attributed the improvement to the uniform,
continuous, and straight nano-scalar network of cellulosic elements
There are three very well-known procedures by which the formation oriented in-plane via the compression of BC film. Chiaoprakobkij et al.
of BC nanocomposites is performed after modifying the original BC [136] formed a porous sponge from the blend of BC and sodium algi-
structure. nate. The BC pellicle was pressed and later mixed with sodium alginate
at different weight ratios in distilled water. The slurry mixture was
3.1.1. BC disintegration placed in Petri dishes and crosslinked with an aqueous CaCl2 solution.
Gea et al. [25] developed nanocomposites by disintegrating a BC The composite exhibited a high mechanical strength, high water uptake
film and then mixing it with apple and radish pulp. The non-disin- ability, and structural stability. Amin et al. [137] combined lyophilized
tegrated BC presented a high tensile modulus (17 GPa), although after BC powder with acrylic acid (AAc) in an aqueous dispersion and sub-
processing the value decreased to 8 GPa. In contrast, the biocomposite sequently exposed the mixture to accelerated electron-beam irradiation,
sheets with apple and radish pulp after BC reinforcement showed an forming BC/AAc hydrogels. The higher the amount of AAc in the gel,
improvement of 2 GPa in Young's modulus (from 4.5 GPa to 6.5 GPa). the higher the AAc degree of polymerization in polyacrylic acid (PAAc).
Feng et al. [76] prepared BC/GO composite by mixing GO and aqueous In addition, those with a higher dose of radiation revealed a higher
suspensions of disintegrated BC at fixed concentrations. The BC/GO extracted weight and gel fraction, which suggests that a higher dose and
mixture was then sonicated, filtered and dried for 24 h at 50 °C to form a higher amount of AAc results in a highly crosslinked and insoluble
films. The films presented up to 20% of Young's modulus increase in network.
comparison with pristine BC.
Nakagaito et al. [135] prepared BC/phenol-formaldehyde

1283
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 7. Undisturbed network methods that promote the use of BC without altering its advantageous original 3-D structure.

3.1.2. Extraction of BC whiskers bonds between glyoxal and BC ribbons, which caused an improvement
A second approach for taking advantage of BC for the development in hydrophobicity. A similar approach was performed by Quero et al.
of nanomaterials is to obtain BC whiskers [138–140]. BC whiskers are [149]. Yang et al. [150] prepared a mixture of poly(vinyl alcohol)
highly crystalline rod-like particles that are extracted by acid hydrolysis (PVA) powder and a BC suspension to produce BC/PVA hydrogels by
of bacterial cellulose microfibrils [141]. Their reinforcement ability lies crosslinking with formaldehyde. Tensile strength and Young's modulus
in their high surface area and excellent mechanical properties were increased after chemical crosslinking took place.
[142,143]. Nevertheless, they should be well separated and distributed
in the matrix [144].
It has been reported that the treatment of BC with acid [145,146] 3.1.4. Bacterial cellulose derivatives based composites
allowed extracting cellulose nanowhiskers effectively. Cellulose whis- Recent works have shown that the synthesis of different derivatives
kers were incorporated into nanofibers of polyethylene oxide (PEO) by of BC by surface modification could open a great variety of potential
the electrospinning process to enhance the mechanical properties of the applications. Several methods performing BC surface modification have
electrospun PEO fibers. The whiskers were partially aligned despite been proposed, including but not limited to carboxymethylation, acet-
some aggregated areas. However, an increase in Young's modulus, ylation, alkylation, and sulfation. Acetylated bacterial cellulose is one
tensile strength, and elongation at break was observed as the con- of the most common BC derivatives used. The acetylation treatment
centration increased [141]. Martínez-Sanz et al. [145] developed hy- replaces the hydroxyl groups of the unmodified BC by less hydrophilic
brid electrospun ethylene vinyl alcohol (copolymer) (EVOH) fibers re- acetyl groups, leading to an improvement in the thermal and moisture
inforced with bacterial cellulose nanowhiskers. They incorporated BC stability of BC-based materials. The optimization of the variables in-
nanowhiskers into 5% (w/v) EVOH solutions, generating hybrid fibers volved in the BC acetylation process such as reaction time, catalyst
by electrospinning which presented an increase in the degree of crys- content and temperature allows tailoring the acetylation extent con-
tallinity. ferred to BC [151]. Goncalves et al. [152] extracted a subjacent lamina
from the basement membrane of a porcine bladder (UBM). The digested
UBM solution was used to coat acetylated bacterial cellulose (ABC),
3.1.3. Crosslinking generating a moderate hydrophobic surface that was advantageous for
Crosslinking is a procedure that links one polymer chain to a chain retinal pigment epithelium cells adhesion and proliferation.
of a different polymer, through covalent or ionic bonds. BC was During carboxymethylation of BC, the cellulose hydroxyl groups are
crosslinked with fibrin in the presence of glutaraldehyde [147]. First, replaced by carboxyl groups, which promote the appearance of co-
bovine fibrin was dissolved in a mixture of 1-butyl-3-methyl-imidazo- ordinate sites. Lin et al. [153] prepared a blend of carboxymethyl
lium chloride (ionic liquid) and dimethyl sulfoxide. Then, the formation bacterial cellulose (CBC)/sodium alginate by an ionic crosslinking with
of the BC/fibrin membrane required the immersion of never-dried BC Ca2+. The composite presented an improvement up to 152% in tensile
sheets in the fibrin solution. Later, the composites were immersed in strength, besides a marked improvement in swelling and thermal
glutaraldehyde solution at 80 °C. The action of glutaraldehyde pro- properties.
moted the crosslinking of hydroxyl groups of BC and the amide groups Lin et al. [154] carried out the first alkylation of BC, by ether-
of fibrin, producing materials with similar tensile strength, modulus ification with alkyl bromide. Qin et al. [155] alkylated BC using alkyl
and time-dependent viscoelastic behavior compared with a small-dia- halide in ionic liquid 1-butyl-3-methylimidazolium chloride and NaH as
meter blood vessel. Castro et al. [148] have reported the crosslinking of the base. The resultant derivatives have both hydrophilic and hydro-
the BC network via glyoxalization with glyoxal. The process started phobic groups on their backbones, whose versatility may result ad-
through medium modification using glyoxal, non-formaldehyde cross- vantageous for a wide variety of applications. Zhu et al. [156] char-
linking agent. The process is started in situ, in the culture medium acterized the properties of sulfated BC (SBC). They found that sulfation
during biosynthesis of cellulose. This allowed the formation of covalent disrupts the crystalline structure of BC, which was reflected in a severe

1284
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

degradation. The careful control of the moisture content in BC allowed nanocomposites. This approach allowed developing a binder-free
to produce SBC with a high degree of substitution. asymmetric supercapacitor, which delivers an energy density of
32.91 W h kg−1 and a maximum power density of 284.63 kW kg−1.
3.2. Undisturbed network Yoon et al. [21] dispersed MWCNTs in a surfactant (cetyl-
trimethylammonium bromide) solution. Then, the BC films were dipped
The importance of an undisturbed coherent fiber network structure in the solution for different immersion rates. The authors reported a
on the mechanical and flow properties of polymer composites has been conductivity of 1.4 × 10−4 S cm−1. Zhou et al. [83] dispersed
confirmed in the past for glass fiber composites [157,158]. Analo- MWCNTs in an absolute ethanol solution at 0.05 wt% concentration to
gously, the purpose of the undisturbed network methods for BC-based coat the BC membrane. These membranes with 13.9 wt% MWCNT
materials development is to take advantage of the highly porous 3-D BC achieved a maximum electrical conductivity of 1.2 S cm−1. Considering
network for the formation of nanocomposites with enhanced properties. a different nanofiller, Yano et al. [106] used silica sols to immerse BC
These methods can be further classified into two approaches: bottom-up hydrogel, allowing the particles to flow to the film and lodge in the
and top-down. spaces between the ribbon-shaped fibrils.
Legnani et al. [165] deposited ITO and SiO2 films onto dried BC
3.2.1. Top-down methods membranes using radio frequency magnetron sputtering, to avoid
3.2.1.1. In situ polymerization. In this process, suitable initiators, heating of the substrate and thus minimization of the membrane strain.
precursors, and monomers are dispersed in the BC network. Then, the These materials can be used as a flexible organic optoelectronic device.
initiators are exposed to an adequate source of excitation, such as heat Yang et al. [166] prepared BC/CdS hybrid nanofibers, which involves
or light. This exposition triggers the in-situ polymerization process that the immersion of BC fibers in ethanol and water (50:50 v/v). The next
forms the nanocomposite. Müller et al. [159] developed BC/PPy step consisted of the hydrothermal reaction of CdCl2 and ethanol-sa-
nanocomposites through in-situ oxidative chemical polymerization. turated BC fibers, and centrifugation leads to a uniform deposition of
Dried BC membranes were immersed in pyrrole aqueous solution of CdS nanoparticles, obtaining BC/CdS hybrid nanofibers. These nanofi-
pyrrole using FeCl3·6H2O as oxidant agent. Figueiredo et al. [160] bers presented high efficiency as photocatalytic and good recyclability.
performed an in situ radical polymerizations of 2-aminoethyl Ccorahua et al. [20] presented a novel processing technique to in-
methacrylate, using N, N-methylene bis(acrylamide) as a crosslinker corporate GO into BC. Once the GO solution was poured over the BC
to obtain films of improved thermal and mechanical properties. Peng gel, and a vacuum pump was turned on, GO was reduced by hydrazine,
et al. [161] immersed BC membranes in a 1% styrene (St) solution with exposing the BC film to hydrazine vapors and forming a thin layer
azobisisobutyronitrile (AIBN) as initiator. The immersed samples were nanocomposite.
pressed at 85 °C for 5 h to carry out the polymerization of the styrene
monomers absorbed in the BC membranes. The BC/PS sheets showed 3.2.2. Bottom-up methods
superior mechanical properties compared to pure PS sheets. Choi et al. 3.2.2.1. Incorporation of phases during BC synthesis. The addition of a
[162] used BC for the development of environmentally compatible ion- second phase for the synthesis of BC fibers implies the modification of
exchange membranes. BC was immersed in benzophenone (BP) the growth medium. Some studies have reported that the inclusion of
methanol solution, used as a photo-initiator, and then irradiated with additives in the culture media promotes the formation of composites
UV light. An AAc solution was added to the activated BC membrane, to [167,168]. Saibuatong and Phisalaphong [169] added Aloe vera gel to
introduce ion-exchangeable groups. A methanol/acetone solution was the culture medium during biosynthesis. With the 30% v/v aloe gel
used to thoroughly clean the resulting acrylic acid-treated bacterial supplement, the nanocomposite film displayed improved properties in
cellulose (AAc-modified BC) membrane. The modified BC/AAc mechanical strength, crystallinity, water absorption capacity, and water
membrane acquired an ion-exchange capacity of 2.5 meq·g−1 and vapor permeability in contrast to unmodified BC films. Grande et al.
greater structural density, as well as a tensile strength of 12 MPa and [23] fabricated BC/HAp nanocomposites by incorporating a mineral
6.0% elongation. Also, Hu et al. [17] synthesized polyaniline/bacterial phase in the static culture during the formation of cellulose microfibrils
cellulose (BC/PAni) nanocomposites by in situ oxidative (Fig. 8). The resultant nanocomposite presented reduced crystallinity
polymerization of aniline. The Young's modulus and tensile strength due to chemical bonds between the components that improve the
of BC decreased from 20 GPa and 357.3 MPa to 5.6 GPa and 95.7 MPa chemical stabilization, and was found to be suitable for biomedical
respectively after polyaniline addition. However, it increased the applications. Gea et al. [170] opted for the direct addition of PVA in an
thermal stability of the flexible membrane and imparted the inoculated medium to prepare nanocomposites. The presence of PVA
composite an electrical conductivity of 5 × 10−2 S cm−1. interrupted hydrogen bonding between cellulose fibrils, yielding a
decrease in Young's modulus but an increase in ductility and work-of-
3.2.1.2. Matrix deposition. BC occurs naturally in the form of a three- fracture.
dimensional nanosized network with a highly porous structure. Matrix Grande et al. [24] prepared BC/starch (corn or potato) nano-
deposition consists of the diffusion of a filler solution into the BC composites in the presence of partly gelatinized starch granules. This
matrix. The diffusion is achieved by immersing BC membranes in an methodology takes advantage of the transport process occurring during
aqueous solution of fillers or by injecting fillers that are soluble in water a “smart” property of starch named gelatinization, which allows the
into the three-dimensional arrangement, forcing nanofillers to remain self-assembly production of the nanocomposite. Starch was placed in
inside the pores through different bonding mechanisms. After the culture medium before a first gelatinization step (to control the
evaporation of the solvent, the filler covers the surface of BC diffusion of polymeric chains into BC network). Then, the BC nanofi-
nanofibers and its internal pores. Later, it is dried or hot pressed to brils grew in the presence of starch. A final hot pressing step permitted
form a strong composite. Typically, matrix deposition is part of a larger to obtain the BC/starch films.
and more complex procedure for nanocomposites formation. Kang et al. The use of water-soluble cellulose derivatives such as methylcellu-
[163] developed all-solid-state flexible supercapacitors based on BC. A lose and CMC enables the slight modification of the culture medium,
BC pellicle was pressed under 10 MPa and later a carbon nanotubes resulting in a decreased crystallinity and crystal size, increased pore
(CNT) ink solution was poured onto the membrane. size and thermal stability. It is also known that increased pore volume
Chen et al. [164] fabricated an asymmetric supercapacitor based on and pore size via in situ modification lead to increased water holding
a 3D nanofibrous carbon network of bacterial cellulose pellicles by capability and water release rate.
annealing for 2 h in an N2 atmosphere. Then, the films were immersed A different approach to incorporate a phase during the preparation
in a 0.1 M KMnO4/0.1 M K2SO4 aqueous solution to obtain the of composites involves their elaboration through the fermentation of

1285
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 8. SEM images corresponding to (a) precipitated HAp powder, (b) original bacterial cellulose network structure, (c) HAp powder inside the bacterial cellulose
nanostructure and (d) broader view of the nanostructure that reflects the final HAp powder distribution.
Extracted from Grande et al. [23].

Gluconacetobacter xylinus in a medium containing cell wall poly- diacrylate (PEGDA) polymer networks. The authors reported that the
saccharides from the hemicellulose or pectin families [171]. It implies mechanical strength was dependent on the weight percent of cross-
reviving and then culturing Gluconacetobacter xylinus in the presence of linked PEGDA in the gel, chain length between crosslinking points, and
desired hemicelluloses and pectins. crosslinking density of PEGDA polymers, with fracture stress and elastic
modulus up to 11.5 MPa and 12 MPa, respectively. The thermo-re-
sponsiveness was preserved upon PEGDA addition, since the composite
3.2.2.2. Double-network hydrogels. Bacterial cellulose can be reinforced
was opaque at low temperature and transparent at high temperature, as
with activated monomers to synthesize double-network (DN)
found for BC/PEG. Yasuda et al. [175] evaluated the properties of 4
hydrogels. Nakayama et al. [129] immersed BC into a gelatin solution
double-network hydrogels, two of which were composed of BC: BC/
and then crosslinked the gelatin with N-(3-dimethyl-aminopropyl)-N′-
PDMAAm (polyacrylamide) and cellulose/gelatin. For the BC/
ethylcarbodiimide hydrochloride (EDC), which activates the carboxyl
PDMAAm composite, the BC film was immersed in an aqueous solution
groups of amino acids. Finally, they obtained BC/gelatin DN gel, with a
of 3 M DMAAm, which was polymerized in the presence of BC gel at
mechanical strength of several megapascals and a frictional coefficient
60 °C for 6 h. For BC/gelatin, BC was immersed in an aqueous solution
of 10−3. Chang et al. [172] prepared double network hydrogels of BC
of gelatin at 50 °C for one week and then immersed in 1-ethyl-(di-
and gelatin. Alkaline treated BC was crosslinked with gelatin using
methylaminopropyl) carbodiimide for chemical crosslinking. BC/ge-
transglutaminase, genipin, and EDC as crosslinking agents. They found
latin showed poor mechanical properties, while BC/PDMAAm resulted
an improvement in both mechanical strength and hydrophilic
resistant to wear, superior in various degrees when compared with
properties of BC, given that gelatin filled the pores and connected the
conventional hydrogels.
3D structure of BC. Additionally, the increase in the concentration of
gelatin enhanced the formation of double-network structures based on
gelatin, which tends to improve the properties of the composite. 4. Applications
Hagiwara et al. [173] developed BC/polyacrylamide (BC/PAAm)
double network hydrogels using N,N′-methylene bisacrylamide as a 4.1. Biomedical
crosslinker. The material presented a tensile fracture stress of
40 ± 10 KPa (similar to ligament strength, 38 ± 10 KPa), which In the same way as other polysaccharides were processed for bio-
suggest potential for the medical field. medical applications [176], BC also found an area in which it can be
Numata et al. [174] developed BC/PEG gels with high mechanical harnessed [177–182]. Soft tissue mimicking materials are of high in-
strength by forming a structure with crosslinked polyethylene glycol terest for the treatment of burns, ulcerative diseases or tissue

1286
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

replacement. PVA is a hydrophilic biocompatible polymer with inter- These properties can be achieved by modifying the specific character-
esting characteristics. It can be crosslinked with BC to form a nano- istics of BC through structural changes, chemical reactions or simply the
composite that exhibits improved lifespan, biocompatibility, and ex- incorporation of a second phase [190]. BC nanocomposites have also
cellent mechanical properties. Millon and Wan [179] developed BC/ been used as drug delivery systems. For instance, a dry BC film im-
PVA nanocomposites and evaluated their capacity to replace cardio- mersed in benzalkonium chloride (an antimicrobial agent) achieved a
vascular tissues. They found that BC/PVA have similar characteristics to drug loading capacity of 0.116 mg/cm2. Trials showed that the drug
cardiovascular tissues. Wang et al. [183] used a freezing-thaw method effects lasted for at least 24 h against contaminated wound flora (Sta-
to prepare a BC/PVA membrane as an artificial cornea replacement. phylococcus aureus and Bacillus subtilis) [177]. Almeida et al. [191]
The results showed that such BC/PVA nanocomposite had high water doped BC membranes with glycerin for topical and transdermal drug
content, high visible light transmittance, UV absorbance, good me- delivery applications. The glycerin presence provided a skin moistur-
chanical properties, and thermal stability. An interesting application izing effect, useful for lesions with dryness such as psoriasis and atopic
involves the formation of BC/polyethylene glycol (PEG) nanocompo- dermatitis.
sites [184]. These BC/PEG nanocomposites showed improved thermal Hydroxypropyl methylcellulose (HPMC) is a well-known tablet ex-
and mechanical properties due to their highly interconnected structure. cipient [192]. Thus, a BC/HPMC composite has been produced adding
In addition, they exhibited good cell adhesion and proliferation prop- HPMC to the culture medium. The trials for using BC based nano-
erties, making them suitable for tissue-engineering and wound dressing composites as tablet excipients show promising results, suggesting that
applications. BC can be used for the delivery of small drug molecules. To complement
The combination of BC with different additives gives rise to mate- this point, BC seems to be an ideal base material due to its capacity to
rials that can be used for bone and cartilage tissue engineering. HAp retain water. Müller et al. [193] grafted BC with polyacrylic acid for
and collagen make up natural bone. Then, given the outstanding os- drug delivery system. The composite showed a pH-sensitive release of
teoconductivity and bioactivity of HAp, it can be applied for tissue BSA (bovine serum albumin, a model protein) at intestinal pH. Besides,
engineering in conjunction with BC [102]. Grande et al. [23] developed those samples with larger pores charged more BSA.
BC/HAp nanocomposites by introducing CMC and a mineral phase in
the culture medium. The CMC addition caused a 50% reduction in the 4.2. Preparation of high strength nanocomposites
diameter of fibers. The authors demonstrated the biocompatibility and
cell viability of the developed nanocomposite using HEK cell cultures. BC has been used as a binder in papers. The small clusters of BC
Saska et al. [122] proposed the combination of collagen and BC, fibers improve strength and durability of pulp paper [194], being viable
forming flexible membranes which showed osteoblastic differentiation to develop high strength paper. Nakagaito et al. [135] developed high-
in vitro. Palaninathan et al. [185] functionalized BC by acetosulfation, strength composites based on bacterial cellulose sheets, by impreg-
verifying cell viability, antioxidant properties, and hemocompatibility nating these with phenolic resin and the use of a compression force of
of the as-constructed composite. 100 MPa. This process produced materials with a bending strength of
The BC nanosized network structure can be used as a starting point 425 MPa and Young's modulus of 28 GPa. The bidimensional orienta-
for specific tasks such as bone regeneration, which require a scaffold tion of the nano-scale BC network structure can be accounted for these
with microsized pores. To address this problem, Bäckdahl et al. [186] high mechanical properties.
placed porogen materials like paraffin wax spheres and starch of var- Additionally, bacterial cellulose has been used in the development
ious grain sizes in the growing medium of Acetobacter xylinum. They of acoustic membranes. Acoustic transducer diaphragms require high
reported that smooth muscle cells migrated to the samples with larger stiffness and low density to maximize the velocity of sound through
pores diameter. Zaborowska et al. [187] incorporated 300–500 μm them. The extremely high Young's modulus and low density that
paraffin wax microspheres into the BC medium to improve cell in- characterizes BC allow the BC-based diaphragms to reach a sound ve-
filtration, by increasing the pore size and introducing osteoprogenitor locity of approximately 5000 m/s [195]. In 1988, the Sony Corporation
cells (Fig. 9). Such a scaffold may be of interest for bone regeneration, developed the first audio speaker diagrams, based on the use of bac-
and it could facilitate osteoblast ingrowth and the formation of mi- terial cellulose (see U.S. Patent 4,742,164).
neralized tissue.
A variety of natural and synthetic polymers are being developed,
4.3. High adsorption composites
containing drug, growth factors, peptides, and other bioactive sub-
stances to enhance wound recovery [188]. In particular, the use of BC
The highly porous structure of BC provides BC-based nanocompo-
as a wound dressing has shown that BC-based dressings prevent
sites with high adsorption capabilities. This property can be useful for
moisture from evaporating and allow for drugs or other bioactive
the removal of toxic components from certain elements, such as heavy
substances to maintain intimate contact with the injured area [189].
metals from wastewater. Stoica-Guzun et al. [196] synthesized bacterial

Fig. 9. (a) Bacterial cellulose-based composite, which presents the interaction of two components of different hierarchy: BC has a nanosized dimension, and the
polymer fibers have a micrometric dimension. (b) Typical pores size of the nanometric BC matrix (scale: 100 μm). (c) Modified microsized pores by the addition of
porogen materials during the growing fermentation (scale: 100 μm). (b) and (c) were extracted from Zaborowska et al. [187].

1287
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

cellulose-magnetite composites for the removal of chromium (VI) at processes. In that sense, it is possible to take advantage of their benefits
different conditions (initial ions concentration, solution pH and solid/ for pollutant abatement in diverse media. Zhang and Qi [208] used BC
liquid ratio upon ions removal) from aqueous solutions. The highest Cr pellicles dipped in a solution of tetra-n-butyl titanate, acetylacetone,
(VI) removal efficiency was observed at pH 4. Chen et al. [197] formed and isopropanol. The resultant material exhibited an enhanced photo-
CBC by incorporating a second phase in the culture medium. The catalytic activity in comparison with an isolated titania network. The
composite exhibited good adsorption performance at pH 4.5, reaching strategy of synthesis is suitable for other metal composites. Zhou et al.
the adsorption equilibrium within 1 h. The maximum adsorption ca- [209] prepared BC nanofibers supported palladium catalyst through 3 h
pacity for copper and lead ions was 12.63 and 60.42 mg/g, respectively. of hydrothermal reduction. The BC/Pd catalyst was highly efficient and
Zhu et al. [56] proposed BC/Fe3O4 nanocomposite for the adsorption of recyclable for standard Heck coupling reaction, with improved thermal
Pb2+, Mn2+, and Cr3+. The adsorption of Pb2+, Mn2+ and Cr3+ ap- stability with regard to pure BC, lower weight loss, and preserving the
proaches 52 mg/g, 26 mg/g and 20 mg/g, respectively for a heavy original structure of Pd and BC. Yang et al. [166] reported the em-
metals ion concentration of 200 mg/l. Lu et al. [198] prepared a new ployment of crystalline cadmium sulfide (CdS) to fabricate BC/CdS via
adsorbent for Cr(VI) removal, ammonium sulfamate-bacterial cellulose a hydrothermal reaction between CdCl2 and thiourea. The resultant
(ASBC). The composite had as main adsorption mechanisms coordina- nanocomposite presented better thermal stability than pure BC. The
tion adsorption and ion exchange, reporting good adsorption capacities photocatalyst efficiency was evaluated through the degradation of
at low pH (1–2), up to 23 mg/g. The effective desorption of Cr(VI) re- methyl orange, obtaining an 82% of degradation and good recycl-
ported by the authors also makes the composite reusable. Yang et al. ability.
[199] prepared BC/poly(m-phenylenediamine) (PmPD) composites for
chromium removal. They performed the BC fibrils functionalization by 4.6. Stimuli responsive materials
mPD in-situ oxidative polymerization. The membranes had an adsorp-
tion capacity of 434.78 mg/g. Oshima et al. [200] proposed the use of Nanogels are crosslinked polymer gels, based on well-dispersed
phosphorylated bacterial cellulose as an adsorbent of metal ions. Shen nanoparticles in an aqueous medium [210]. They present environ-
et al. [201] prepared BC/diethylenetriamine nanocomposites as mem- mental sensitivity, i.e., response to changes in temperature, pH, lumi-
branes for Cu2+ and Pb2+ adsorption. The adsorption observed was a nance, chemical, and physical stimuli and other external factors. One of
fast process which reached the adsorption equilibrium within 2 h. The the most investigated thermosensitive nanogels is poly(N-iso-
adsorption kinetics closely followed the pseudo-second-order kinetic propylacrylamide) (PNIPAM) [211]. Halake and Lee [212] used fibers
model, indicating the importance of chemical adsorption in the process. of BC as nanostructures, aligned micropores as microstructures and
The nanocomposite presented the best adsorption capability at a pH of then performed in situ UV photopolymerization to immobilize both
4.5, with 63.09 and 87.41 mg/g for Cu and Pb respectively. components into a PNIPAMs network. The combination enhanced the
volume transition, allowed fast water infiltration (ideal for super ab-
4.4. Optical materials sorbent applications) but reduced the elastic modulus. BC whiskers/
poly(N-isopropylacrylamide-co-butyl methacrylate) (PNB) nanogel
Optical materials need to have good transparency, good flexibility, complexes, designated as BC/PNB, were elaborated in [213] by soap-
dimensional stability, and be free from scattering. Nanostructures with free emulsion polymerization based on PNIPAM and poly(N-iso-
components less than 1/10 of wavelength in size will not present propylacrylamide-co-butyl methacrylate) (PNB) nanogels. BC con-
scattering [202]. Thus, nanocomposites based on BC with fibers dia- tributed to enhancing the poor mechanical properties of isolated PNB,
meter in the range 40–70 nm, will display excellent optical properties, yielding good biosafety. In addition, the nanomaterial retained the
good flexibility, and dimensional stability [203]. Yano et al. [204] good thermo-sensitivity of PNB, with easy flow at low temperatures and
impregnated dried BC membranes with acrylic resin. The resulting gel formation at high temperatures, being suitable for vascular embo-
nanocomposite had a fiber content of up to 70% and showed a small lization interventional therapy. On the other hand, the addition of AAc
loss of transparency (less than 10%), significantly low thermal expan- makes hydrogels to become thermo- and pH-responsive. The exposure
sion coefficient and good mechanical properties compared with en- to electron-beam irradiation of BC and AAc permitted their combina-
gineering plastics. Nogi et al. [205] prepared BC/tricyclodecane di- tion at different doses [137]. The resultant hydrogel presented a mac-
methanol dimethacrylate (TCDDMA) nanocomposites with different roporous structure, with pore size decreasing when increasing the AAc
percentages of BC. They reported that the addition of 7.4 wt% of bac- content and irradiation dose. They were pH-responsive, suggesting a
terial cellulose nanofibers caused light transmittance deterioration of possible application in temperature-controlled delivery.
only 2.4% but reduced the coefficient of thermal expansion of acrylic
resin from 86 × 10−6 to 38 × 10−6 K−1. 4.7. Sensors
BC nanofibers were acetylated to enhance the properties of optically
transparent composites of acrylic resin reinforced with the nanofibers The development of BC based sensors has taken advantage of its
[206]. They found that acetylation reduced the refractive index of BC large specific surface area, the number of surface hydroxyl groups, high
and the loss in regular transmittance of the material (from 13% to 3.4% water absorption capacity and water holding capacity [214]. BC na-
at a fiber content of 63%). It also reduced hygroscopicity, and water nofibers have been used to cover a quartz crystal microbalance (QCM)
absorption was found to be less than 0.5%. Besides, the coefficient of for the preparation of a humidity sensor. When the humidity of the
thermal expansion obtained was around 1 × 10−6 K−1. Later, Fer- testing chamber rose, the weight increase of BC was registered. Thus, it
nandes et al. [207] developed films based on BC and chitosan, ob- was feasible to fabricate a simple, highly stable, sensitive, and low-cost
taining a material with a transmittance of 90% in the range of humidity sensor based on BC nanofibrous coated QCM [214]. A similar
400–700 nm (see Fig. 10). The addition of BC to unfilled chitosan films procedure allowed for preparing a formaldehyde sensor using BC and
promoted an increase in Young's modulus and a reduction in the QCM [215], coating BC with PEI. The hydroxyl groups of BC and the
elongation at break value, in addition to reasonable thermal stability amide groups of PEI permitted the formation of hydrogen bonds. The
and low O2 permeability. nanofibrous BC/PEI network was successfully used for the detection of
formaldehyde, with PEI acting as the detective material. The sensor
4.5. Catalytic materials exhibited good reversibility, reproducibility and a linear relationship
with the increase of formaldehyde concentrations (concentration range
Materials with porous nanostructures are an alternative for the de- of 1–100 ppm at room temperature).
velopment of heterogeneous catalysts and membranes for separation Wang et al. [216] reported a different approach for the preparation

1288
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

Fig. 10. Nano-nano composites based on chitosan matrices and bacterial cellulose. (a) High molecular weight membrane of chitosan presents a high transmittance.
The addition of 5% of BC did not affect the results. (b) The addition of 10% of chitosan reduced the transmittance.
Extracted from Fernandes et al. [207].

of a BC/Au sensor. They performed the synthesis of gold nanoparticles health and decreases the risk of chronic diseases such as obesity, dia-
in a suspension of BC. Heme proteins such as horseradish peroxidase, betes, and cardiovascular disease [221]. Similarly, it can be used as an
hemoglobin (Hb) and myoglobin (Mb) were successfully immobilized additive to produce low-calorie food. Lin et al. [222] processed BC with
on the surface of the BC/Au surface. The immobilized heme proteins an alkali treatment, increasing its water-holding capacity. The resultant
showed electrocatalytic activities to the reduction of H2O2 in the pre- composite (designated as alkaline treated-nata) was added to surimi,
sence of the mediator hydroquinone (HQ). The amperometric hydrogen finding that the BC properties were appropriate for its use as a fat re-
peroxide biosensor prepared showed biocatalytic activity with good placement and an additional dietary source. Chau et al. [223] found
sensitivity, low detection limit and fast response to hydrogen peroxide. that the administration of BC to hamsters decreased the concentrations
Wang et al. [217] followed a similar procedure to develop a BC/Au of serum triglyceride, serum total cholesterol, and liver cholesterol,
glucose biosensor. being considered as an alternative for gelatin or similar products.
Okiyama et al. [224] have analyzed the effect of BC on the rheology of
4.8. Membranes for separation processes food. They found that BC, unlike xanthan gum, prevents the pre-
cipitation of cocoa in chocolate drinks by trapping it in the micro-
The intrinsic properties of BC also give rise to its application as an fibrillar mesh, acting as an excellent suspending agent. BC also im-
agent for separation of elements, filtration, dialysis or to favor ions proved the mechanical properties of pasty condiments by reducing its
exchange between two composites. Phisalaphong et al. [218] dissolved stickiness. BC can be used as a stabilizer for ice cream since it can be
3 wt% BC in an aqueous solution made of 4 wt% NaOH and 3 wt% urea. considered similar to the commonly used gum for the same purpose. BC
Then, the BC slurry was cooled at −5 °C for 12 h, later centrifuged at has also been used in tofu body-reinforcement. Tofu's fragility is a big
10 °C for 30 min. The solution was then mixed with a 3 wt% sodium problem for its transportation; however, with a minimum percentage of
alginate solution and finally coagulated in 5 wt% CaCl2 and 1% HCl BC, its mechanical properties improved significantly.
solution. Although the mechanical properties of BC-based composite Also, bacterial cellulose has found applications in smart and active
decreased, the degree of swelling in water improved. Since it exhibits a packaging. Bacterial cellulose-based edible antimicrobial films were
homogeneous nanoporous structure, chemical stability, and water ab- developed using bovine lactoferrin as the active component [225].
sorption capability, the authors proposed its use for separation pro- These functionalized films reduced the viability of E. coli and S. aureus,
cesses. He et al. [219] explored the adsorption capacity of BC/silica, and were proposed for being used in direct contact with highly per-
built by vacuum infiltration. The material exhibited superelasticity and ishable foods. Jipa et al. [226] developed BC based films incorporating
recyclable compressibility, hydrophobicity with a contact angle of 152°, sorbic acid (SA) as an antimicrobial agent. Monolayer films, prepared
oil binding capacity of 10 times its weight and an oil-retrieving capa- using powdered BC (BCP) and poly(vinyl alcohol) (PVA), were coated
city. with BC membrane to obtain multilayer films. Tests indicated that both
Dubey et al. [220] developed a BC/chitosan membrane in order to SA and BCP concentration influenced sensitivity to water, release rate
obtain the separation of ethanol/water azeotrope (EtOH/H2O). In and antimicrobial ability of mono and multilayer films. Using E. coli -
contrast to the blend of PVA and chitosan (which dissolve at high water one of the most important pathogens for testing antimicrobial proper-
concentration), the BC/chitosan membrane remained unchanged. Also, ties of films, they reported a diffusion coefficient for the antimicrobial
it showed better thermal stability, dimensional stability, and superior agent of 10–12 m2 cm−1 for monolayer films, being higher than for
mechanical properties. Choi et al. [162] prepared BC/AAc (acrylic acid) multilayer ones. Also, the SA concentration and the water solubility of
nanocomposite membranes with ion-exchange capacities. the films influenced the effectiveness of the antimicrobial properties
[226].
Kuswandi et al. [227] immobilized methyl red onto a bacterial
4.9. Food applications
cellulose membrane by the absorption method, to develop a novel
sticker sensor. The relationship between the color change of the sensor
Food industry also takes advantage of BC, since it can form hydro-
and storage time of chicken followed a similar trend, suggesting a
gels with good rheological properties. It is feasible to perform the BC
possible application for assessing chicken cuts' freshness. Similarly, it
growth medium modification to give flavor, color, texture, and shape to
was reported that a BC/curcumin membrane responded with visible
cellulose produced by the bacteria, making it usable in food.
color changes to volatile amines released during fish spoilage [228] and
BC is a type of dietary fiber, which offers benefits to the digestive

1289
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

that bromophenol blue/bacterial cellulose worked as a color indicator dimensions) lead to the improvement of one or several characteristics of
for assessing the freshness state of the guava fruit [229]. In the same BC-based nanocomposites, such as mechanical properties, degradation
line, Pourjavaher et al. [230] developed bacterial cellulose-based pH ratio, water absorption uptake, electrical conductivity, thermal stabi-
indicator by immersing the films in an anthocyanins solution extracted lity, and optical characteristics. Bacterial cellulose presents a nanosized
from Brassica oleracea. BC-diluted anthocyanins films demonstrated a 3-D structure, and some fillers can also have nanometric dimensions.
high pH-responsive behavior when exposed to pH 2–10. The interaction between these two phases can be described as an in-
teraction between two nanometric supra-molecular structures. The re-
4.10. Energy storage sultant composite can be regarded as an all-nano or nano-nano mate-
rial.
The combination of BC with conductive nanomaterials can lead to In addition, many practical procedures can be used to elaborate
the development of devices used for energy storage applications. The these all-nano composites. Based on them, this review has proposed a
ability of BC to catalyze the precipitation of palladium generates classification that takes into consideration the final state of the BC
structures with a high surface area. In that sense, the BC/Pd materials matrix after the incorporation of the reinforcements. They can be
can have applications in electronic devices [231]. BC was found to be classified into two clearly identifiable clusters: disturbed or undisturbed
suitable for the construction of polyelectrolyte membranes and fuel cell network methods. The former generally involves the use of a disin-
development. Yang et al. [73] used platinum to develop BC/Pt using an tegrated BC network or single BC fibrils, which require the incorpora-
in situ chemical-reduction method, obtaining a catalyst with high tion of a second phase to form the composite. The latter keeps intact the
electrocatalytic activity. By doping the BC films with proton acid, the original BC matrix, taking advantage of its structural properties and
matrix proton conductivity increases notably, indicating the BC avail- finally blending it with reinforcing nanoparticles. Despite the differ-
ability to be explored as membrane in fuel cells. ence, both methods involve BC interaction with various fillers, as well
In addition to mechanical strength, the materials used for energy as reinforcement of synthetic polymers with BC nanofibers.
devices should exhibit flexibility for technological applications. Thus, Furthermore, the undisturbed network methods can be sub-classified in
the development of electrically conductive and stretchable membranes turn into bottom-up and top-down approaches. Bottom-up approaches
is of special interest. Pyrolyzed bacterial cellulose, composed of inter- usually consist of making an initial modification to the culture medium
welded ultrathin carbon nanofibrils, can be an alternative to produce a of the Acetobacter bacteria, adding the nanoreinforcements. As the 3-D
mechanically robust three-dimensional conductive network [232]. matrix is formed, the nanoparticles will be incorporated automatically.
Pyrolyzed BC/polydimethylsiloxane pellicles were produced using BC Top-down approaches imply the incorporation of the nanoreinforce-
as a precursor. These exhibited an electrical conductivity of ments on the bacterial cellulose 3-D matrix already formed, using ca-
0.2–0.41 S cm−1, maintaining their electromechanical properties when pillarity or in situ polymerization to absorb them.
subjected to high tensile and bending strain [233]. BC nanocomposites have found a variety of applications in several
Constructing asymmetric supercapacitors based on BC is feasible. areas. Their porosity, nontoxic biocompatibility, water holding capa-
Chen et al. [164] developed a supercapacitor by coating BC pellicles city, and high strength make them suitable for applications including
with MnO2 (BC/MnO2) to act as the positive electrode and then coating but not limited to high strength materials, catalytic materials, optical
BC with nitrogen to act as the negative electrode using a green ap- materials, sensors, wound dressing, bone tissue engineering, food ap-
proach. The device was reversibly charged/discharged, delivering an plications and energy storage, among others, which were explained in
energy density of 32.91 W h kg−1 with high cycling stability. detail in this review. In consequence, BC turns out to be a functional
material with advantageous properties already tested for technological
4.11. Others and day-to-day applications. The development on a large scale and
therefore the generic use of these nano-nano composites is still a
The cellulose synthesized by the Gluconacetobacter bacteria has been pending aspect, and it is expected that due to its low impact on the
used to develop a model for plant cell walls [234–236]. Furthermore, it environment and health, in the midterm it will be a fulfilled objective.
is feasible to use BC to study the plant cell expansive growth. Initially,
researchers presumed that the plant cells growth occurred due to the Acknowledgements
presence of a wall loosening agent, but not due to the cellulose network
by itself. Based on their work with bacterial cellulose, Torres et al. The authors would like to thank the Vice-rectorate of Research of
[237] noticed that the BC network presents certain mechanical prop- the Pontificia Universidad Católica del Peru (VRI-PUCP) for financial
erties that offer a satisfactory explanation to the wall stress relaxation support.
phenomena (which gives rise to plant cell growth). They suggested that
the wall stress relaxation was determined by the cellulose network itself References
but not for a wall loosening agent. That is, BC displays reversible stress
softening and stress recovery, which is consistent with the behavior of [1] M.P. Coughlan, Biochem. Soc. Trans. 13 (1985) 405–406.
plant cells when growing, since the cells remain unaltered for a given [2] J. Pérez, J. Muñoz-Dorado, T. de la Rubia, J. Martinez, Int. Microbiol. 5 (2002)
53–63.
range of internal pressure until reaching a critical threshold, after [3] A.P. Mathew, A. Chakraborty, K. Oksman, M. Sain, Cellulose Nanocomposites:
which they expand. This behavior can also explain the mechanical Processing, Characterization and Properties, American Chemical Society (ACS),
“safety mechanism” under stress reported for plant and animal cells Washington DC USA, 2006, pp. 114–131.
[4] B. Madsen, E.K. Gamstedt, Adv. Mater. Sci. Eng. 2013 (2013) 1–14.
which preserves their existence [237]. [5] M. Iguchi, S. Yamanaka, A. Budhiono, J. Mater. Sci. 35 (2000) 261–270.
[6] M. Shoda, Y. Sugano, Biotechnol. Bioprocess Eng. 10 (2005) 1–8.
5. Conclusions and remarks [7] H. Bäckdahl, G. Helenius, A. Bodin, U. Nannmark, B.R. Johansson, B. Risberg,
P. Gatenholm, Biomaterials 27 (2006) 2141–2149.
[8] E. Vandamme, S. De Baets, A. Vanbaelen, K. Joris, P. De Wulf, Polym. Degrad.
Bacterial cellulose emerges as a versatile material for future appli- Stab. 59 (1998) 93–99.
cations in various areas. Its availability, 3-D network structure, ex- [9] F. Schierbaum, Starch-Starke 57 (2005) 453.
[10] W.K. Czaja, D.J. Young, M. Kawecki, R.M. Brown, Biomacromolecules 8 (2007)
cellent mechanical properties, and the ability to host reinforcements to
1–12.
achieve synergistic and superior properties have opened the possibility [11] S. Koizumi, Z. Yue, Y. Tomita, T. Kondo, H. Iwase, D. Yamaguchi, T. Hashimoto,
of more constant and extensive uses. Eur. Phys. J. E 26 (2008) 137–142.
We have shown how the use of different nanofillers (conducting [12] R.H. Atalla, D.L. VanderHart, Science 223 (1984) 283–286.
[13] K.-Y. Lee, G. Buldum, A. Mantalaris, A. Bismarck, Macromol. Biosci. 14 (2014)
polymers, metal, graphene, ceramics, and bio-materials of nanometric

1290
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

10–32. [62] C. Carlson, S.M. Hussain, A.M. Schrand, L.K. Braydich-Stolle, K.L. Hess, R.L. Jones,
[14] K. Gelin, A. Bodin, P. Gatenholm, A. Mihranyan, K. Edwards, M. Strømme, J.J. Schlager, J. Phys. Chem. B 112 (2008) 13608–13619.
Polymer 48 (2007) 7623–7631. [63] J. Wu, Y. Zheng, W. Song, J. Luan, X. Wen, Z. Wu, X. Chen, Q. Wang, S. Guo,
[15] J. Guo, J.M. Catchmark, Carbohydr. Polym. 87 (2012) 1026–1037. Carbohydr. Polym. 102 (2014) 762–771.
[16] C.J. Grande, F.G. Torres, C.M. Gomez, O.P. Troncoso, J. Canet-Ferrer, J. Martinez- [64] M.-C. Daniel, D. Astruc, Chem. Rev. 104 (2004) 293–346.
Pastor, Polym. Polym. Compos. 16 (2008) 181. [65] M. Chen, H. Kang, Y. Gong, J. Guo, H. Zhang, R. Liu, ACS Appl. Mater. Interfaces 7
[17] W. Hu, S. Chen, Z. Yang, L. Liu, H. Wang, J. Phys. Chem. B 115 (2011) 8453–8457. (2015) 21717–21726.
[18] D. Müller, J. Mandelli, J. Marins, B. Soares, L. Porto, C. Rambo, G. Barra, Cellulose [66] T. Ishida, H. Watanabe, T. Bebeko, T. Akita, M. Haruta, Appl. Catal. A Gen. 377
19 (2012) 1645–1654. (2010) 42–46.
[19] L. Ma, R. Liu, H. Niu, M. Zhao, Y. Huang, Compos. Sci. Technol. 137 (2016) 87–93. [67] X. Tan, W. Deng, M. Liu, Q. Zhang, Y. Wang, Chem. Commun. (2009) 7179–7181.
[20] R. Ccorahua, O.P. Troncoso, S. Rodriguez, D. Lopez, F.G. Torres, Carbohydr. [68] X. Zhou, Z. Zhao, Y. He, Y. Ye, J. Zhou, J. Zhang, X. Wang, Cellulose 25 (2018)
Polym. 171 (2017) 68–76. 3941–3953.
[21] S.H. Yoon, H.-J. Jin, M.-C. Kook, Y.R. Pyun, Biomacromolecules 7 (2006) [69] T. Zhang, W. Wang, D. Zhang, X. Zhang, Y. Ma, Y. Zhou, L. Qi, Adv. Funct. Mater.
1280–1284. 20 (2010) 1152–1160.
[22] M. Ul-Islam, T. Khan, W.A. Khattak, J.K. Park, Cellulose 20 (2013) 589–596. [70] Z. Liu, M. Li, L. Turyanska, O. Makarovsky, A. Patane, W. Wu, S. Mann, Chem.
[23] C.J. Grande, F.G. Torres, C.M. Gomez, M.C. Bañó, Acta Biomater. 5 (2009) Mater. 22 (2010) 2675–2680.
1605–1615. [71] S. Peng, L. Fan, W. Rao, Z. Bai, W. Xu, J. Xu, J. Mater. Sci. 52 (2017) 1930–1942.
[24] C.J. Grande, F.G. Torres, C.M. Gomez, O.P. Troncoso, J. Canet-Ferrer, J. Martínez- [72] S. Chen, B. Zhou, W. Hu, W. Zhang, N. Yin, H. Wang, Carbohydr. Polym. 92 (2013)
Pastor, Mater. Sci. Eng. C 29 (2009) 1098–1104. 1953–1959.
[25] S. Gea, F. Torres, O. Troncoso, C. Reynolds, F. Vilasecca, M. Iguchi, T. Peijs, Int. [73] J. Yang, D. Sun, J. Li, X. Yang, J. Yu, Q. Hao, W. Liu, J. Liu, Z. Zou, J. Gu,
Polym. Process. 22 (2007) 497–501. Electrochim. Acta 54 (2009) 6300–6305.
[26] S. Yamanaka, K. Watanabe, N. Kitamura, M. Iguchi, S. Mitsuhashi, Y. Nishi, [74] D. Sun, J. Yang, J. Li, J. Yu, X. Xu, X. Yang, Appl. Surf. Sci. 256 (2010) 2241–2244.
M. Uryu, J. Mater. Sci. 24 (1989) 3141–3145. [75] R.T. Olsson, M.A. Samir, G. Salazar-Alvarez, L. Belova, V. Ström, L.A. Berglund,
[27] X. Chen, F. Yuan, H. Zhang, Y. Huang, J. Yang, D. Sun, J. Mater. Sci. 51 (2016) O. Ikkala, J. Nogues, U.W. Gedde, Nat. Nanotechnol. 5 (2010) 584–588.
5573–5588. [76] Y. Feng, X. Zhang, Y. Shen, K. Yoshino, W. Feng, Carbohydr. Polym. 87 (2012)
[28] Y. Qiu, L. Qiu, J. Cui, Q. Wei, Mater. Sci. Eng. C 59 (2016) 303–309. 644–649.
[29] A. Svensson, E. Nicklasson, T. Harrah, B. Panilaitis, D. Kaplan, M. Brittberg, [77] M. Sanchis, M. Carsí, C. Gómez, M. Culebras, K. Gonzales, F. Torres, Carbohydr.
P. Gatenholm, Biomaterials 26 (2005) 419–431. Polym. 157 (2017) 353–360.
[30] S. Zang, R. Zhang, H. Chen, Y. Lu, J. Zhou, X. Chang, G. Qiu, Z. Wu, G. Yang, [78] H. Si, H. Luo, G. Xiong, Z. Yang, S.R. Raman, R. Guo, Y. Wan, Macromol. Rapid
Mater. Sci. Eng. C 46 (2015) 111–117. Commun. 35 (2014) 1706–1711.
[31] J. Juntaro, M. Pommet, G. Kalinka, A. Mantalaris, M.S. Shaffer, A. Bismarck, Adv. [79] H. Luo, J. Dong, X. Xu, J. Wang, Z. Yang, Y. Wan, Compos. A: Appl. Sci. Manuf.
Mater. 20 (2008) 3122–3126. 109 (2018) 290–297.
[32] M. Pommet, J. Juntaro, J.Y. Heng, A. Mantalaris, A.F. Lee, K. Wilson, G. Kalinka, [80] J.M. Gutiérrez-Hernández, D.M. Escobar-García, A. Escalante, H. Flores,
M.S. Shaffer, A. Bismarck, Biomacromolecules 9 (2008) 1643–1651. F.J. González, P. Gatenholm, G. Toriz, Mater. Sci. Eng. C 75 (2017) 445–453.
[33] K.-Y. Lee, K.K. Ho, K. Schlufter, A. Bismarck, Compos. Sci. Technol. 72 (2012) [81] Y. Liu, J. Zhou, E. Zhu, J. Tang, X. Liu, W. Tang, J. Mater. Chem. C 3 (2015)
1479–1486. 1011–1017.
[34] C.M. Vu, D.D. Nguyen, T.D. Pham, L.T. Pham, H.J. Choi, Polym. Test. 61 (2017) [82] A.K. Geim, K.S. Novoselov, Nat. Mater. 6 (2007) 183–191.
150–161. [83] T. Zhou, D. Chen, J. Jiu, T. Nge, T. Sugahara, S. Nagao, H. Koga, M. Nogi,
[35] S. Phomrak, M. Phisalaphong, J. Nanomater. (2017) 1–9, https://doi.org/10. K. Suganuma, X. Wang, X. Liu, P. Cheng, T. Wang, D. Xiong, Express Polym Lett 7
1155/2017/4739793. (2013) 756–766.
[36] H. Shirakawa, E.J. Louis, A.G. MacDiarmid, C.K. Chiang, A.J. Heeger, Journal of [84] W. Shao, S. Wang, H. Liu, J. Wu, R. Zhang, H. Min, M. Huang, Carbohydr. Polym.
the chemical society, Chem. Commun. (1977) 578–580. 138 (2016) 166–171.
[37] Z. Shi, G.O. Phillips, G. Yang, Nanoscale 5 (2013) 3194–3201. [85] S. Pei, H.-M. Cheng, Carbon 50 (2012) 3210–3228.
[38] E. Genies, A. Boyle, M. Lapkowski, C. Tsintavis, Synth. Met. 36 (1990) 139–182. [86] W. Shao, H. Liu, X. Liu, S. Wang, R. Zhang, RSC Adv. 5 (2015) 4795–4803.
[39] H. Wang, E. Zhu, J. Yang, P. Zhou, D. Sun, W. Tang, J. Phys. Chem. C 116 (2012) [87] Y. Liu, J. Zhou, J. Tang, W. Tang, Chem. Mater. 27 (2015) 7034–7041.
13013–13019. [88] H. Luo, J. Dong, F. Yao, Z. Yang, W. Li, J. Wang, Y. Wan, Nano Micro Lett. 10
[40] J.A. Marins, B.G. Soares, K. Dahmouche, S.J. Ribeiro, H. Barud, D. Bonemer, (2018) 42.
Cellulose 18 (2011) 1285–1294. [89] M. Acik, G. Lee, C. Mattevi, M. Chhowalla, K. Cho, Y. Chabal, Nat. Mater. 9 (2010)
[41] Y. Wan, J. Li, Z. Yang, H. Ao, L. Xiong, H. Luo, Curr. Appl. Phys. 18 (2018) 840.
933–940. [90] H.A. Becerril, J. Mao, Z. Liu, R.M. Stoltenberg, Z. Bao, Y. Chen, ACS Nano 2 (2008)
[42] M. Lay, I. González, J.A. Tarrés, N. Pellicer, K.N. Bun, F. Vilaseca, Eur. Polym. J. 463–470.
91 (2017) 1–9. [91] C. Gómez-Navarro, R.T. Weitz, A.M. Bittner, M. Scolari, A. Mews, M. Burghard,
[43] S. Li, D. Huang, J. Yang, B. Zhang, X. Zhang, G. Yang, M. Wang, Y. Shen, Nano K. Kern, Nano Lett. 7 (2007) 3499–3503.
Energy 9 (2014) 309–317. [92] S. Stankovich, D.A. Dikin, R.D. Piner, K.A. Kohlhaas, A. Kleinhammes, Y. Jia,
[44] S. Peng, L. Fan, C. Wei, H. Bao, H. Zhang, W. Xu, J. Xu, Cellulose 23 (2016) Y. Wu, S.T. Nguyen, R.S. Ruoff, Carbon 45 (2007) 1558–1565.
2639–2651. [93] G. Williams, B. Seger, P.V. Kamat, ACS Nano 2 (2008) 1487–1491.
[45] D. Muller, C.R. Rambo, L.M. Porto, W.H. Schreiner, G.M. Barra, Carbohydr. Polym. [94] O. Akhavan, E. Ghaderi, J. Phys. Chem. C 113 (2009) 20214–20220.
94 (2013) 655–662. [95] A.G. Nandgaonkar, Q. Wang, K. Fu, W.E. Krause, Q. Wei, R. Gorga, L.A. Lucia,
[46] A. Bayer, Synth. Met. 41 (1991) 831–836. Green Chem. 16 (2014) 3195–3201.
[47] M. Dietrich, J. Heinze, G. Heywang, F. Jonas, J. Electroanal. Chem. 369 (1994) [96] J.H. Sung, H.S. Kim, H.-J. Jin, H.J. Choi, I.-J. Chin, Macromolecules 37 (2004)
87–92. 9899–9902.
[48] L. Groenendaal, F. Jonas, D. Freitag, H. Pielartzik, J.R. Reynolds, Adv. Mater. 12 [97] S.H. Yoon, M. Kang, W.-I. Park, H.-J. Jin, Mol. Cryst. Liq. Cryst. 464 (2007)
(2000) 481–494. 103–685.
[49] S. Khan, M. Ul-Islam, W.A. Khattak, M.W. Ullah, J.K. Park, Carbohydr. Polym. 127 [98] S. Li, D. Huang, B. Zhang, X. Xu, M. Wang, G. Yang, Y. Shen, Adv. Energy Mater. 4
(2015) 86–93. (2014) 1301655.
[50] S.-S. Kim, J.-H. Jeon, C.-D. Kee, I.-K. Oh, Smart Mater. Struct. 22 (2013) 085026. [99] H. Aoki, Medical Applications of Hydroxyapatite, Ishiyaku Euro America, Tokio,
[51] A.N. Aleshin, A.S. Berestennikov, P.S. Krylov, I.P. Shcherbakov, V.N. Petrov, St. Louis, 1994, pp. 13–74.
I.N. Trapeznikova, R.I. Mamalimov, A.K. Khripunov, A.A. Tkachenko, Synth. Met. [100] T. Goto, T. Kojima, T. Iijima, S. Yokokura, H. Kawano, A. Yamamoto, K. Matsuda,
199 (2015) 147–151. J. Orthop. Sci. 6 (2001) 444–447.
[52] Y. Bu, M. Cao, Y. Jiang, L. Gao, Z. Shi, X. Xiao, Y. Shen, Electrochim. Acta 271 [101] Y. Shinto, A. Uchida, F. Korkusuz, N. Araki, K. Ono, Bone Joint J. 74 (1992)
(2018) 624–631. 600–604.
[53] N. Colaneri, D. Bradley, R. Friend, P. Burn, A. Holmes, C. Spangler, Phys. Rev. B 42 [102] Y. Wan, Y. Huang, C. Yuan, S. Raman, Y. Zhu, H. Jiang, F. He, C. Gao, Mater. Sci.
(1990) 11670. Eng. C 27 (2007) 855–864.
[54] A.N. Aleshin, I. Shcherbakov, A. Khripunov, A. Tkachenko, I. Trapeznikova, [103] K.A. Zimmermann, J.M. LeBlanc, K.T. Sheets, R.W. Fox, P. Gatenholm, Mater. Sci.
V. Petrov, Flexi. Print. Electron. 2 (2017) 035004. Eng. C 31 (1) (2011) 43–49.
[55] W. Zhang, S. Chen, W. Hu, B. Zhou, Z. Yang, N. Yin, H. Wang, Carbohydr. Polym. [104] S. Saska, H. Barud, A. Gaspar, R. Marchetto, S.J.L. Ribeiro, Y. Messaddeq, Int. J.
86 (2011) 1760–1767. Biomater. 2011 (2011) 1–8.
[56] H. Zhu, S. Jia, T. Wan, Y. Jia, H. Yang, J. Li, L. Yan, C. Zhong, Carbohydr. Polym. [105] S.A. Hutchens, R.S. Benson, B.R. Evans, H.M. ONeill, C.J. Rawn, Biomaterials 27
86 (2011) 1558–1564. (2006) 4661–4670.
[57] N. Sriplai, W. Mongkolthanaruk, S.J. Eichhorn, S. Pinitsoontorn, Carbohydr. [106] S. Yano, H. Maeda, M. Nakajima, T. Hagiwara, T. Sawaguchi, Cellulose 15 (2008)
Polym. 192 (2018) 251–262. 111–120.
[58] T. Maneerung, S. Tokura, R. Rujiravanit, Carbohydr. Polym. 72 (2008) 43–51. [107] H. Maeda, M. Nakajima, T. Hagiwara, T. Sawaguchi, S. Yano, J. Mater. Sci. 41
[59] W. Hu, S. Chen, X. Li, S. Shi, W. Shen, X. Zhang, H. Wang, Mater. Sci. Eng. C 29 (4) (2006) 5646–5656.
(2009) 1216–1219. [108] J. Cai, S. Liu, J. Feng, S. Kimura, M. Wada, S. Kuga, L. Zhang, Angew. Chem. 124
[60] K.-H. Cho, J.-E. Park, T. Osaka, S.-G. Park, Electrochim. Acta 51 (2005) 956–960. (2012) 2118–2121.
[61] P. Dallas, V.K. Sharma, R. Zboril, Adv. Colloid Interf. Sci. 166 (2011) 119–135. [109] H. Barud, R. Assuncao, M. Martines, J. Dexpert-Ghys, R. Marques, Y. Messaddeq,

1291
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

S. Ribeiro, J. Sol-Gel Sci. Technol. 46 (2008) 363–367. [159] D. Müller, C. Rambo, D. Recouvreux, L. Porto, G. Barra, Synth. Met. 161 (2011)
[110] H. Sai, L. Xing, J. Xiang, L. Cui, J. Jiao, C. Zhao, Z. Li, F. Li, J. Mater. Chem. A 1 106–111.
(2013) 7963–7970. [160] A.R. Figueiredo, A.G. Figueiredo, N.H. Silva, A. Barros-Timmons, A. Almeida,
[111] A. Stoica-Guzun, M. Stroescu, S. Jinga, I. Jipa, T. Dobre, L. Dobre, Ultrason. A.J. Silvestre, C.S. Freire, Carbohydr. Polym. 123 (2015) 443–453.
Sonochem. 19 (2012) 909–915. [161] K. Peng, B. Wang, S. Chen, C. Zhong, H. Wang, J. Macromol. Sci. Part B Phys. 50
[112] S. Shi, S. Chen, X. Zhang, W. Shen, X. Li, W. Hu, H. Wang, J. Chem. Technol. (2011) 1921–1927.
Biotechnol. 84 (2009) 285–290. [162] Y.-J. Choi, Y. Ahn, M.-S. Kang, H.-K. Jun, I.S. Kim, S.-H. Moon, J. Chem. Technol.
[113] M. Stroescu, A. Stoica-Guzun, S.I. Jinga, T. Dobre, I.M. Jipa, L.M. Dobre, Korean J. Biotechnol. 79 (2004) 79–84.
Chem. Eng. 29 (2012) 1216–1223. [163] Y.J. Kang, S.-J. Chun, S.-S. Lee, B.-Y. Kim, J.H. Kim, H. Chung, S.-Y. Lee, W. Kim,
[114] G. Serafica, R. Mormino, H. Bungay, Appl. Microbiol. Biotechnol. 58 (2002) ACS Nano 6 (2012) 6400–6406.
756–760. [164] L.-F. Chen, Z.-H. Huang, H.-W. Liang, Q.-F. Guan, S.-H. Yu, Adv. Mater. 25 (2013)
[115] A. Stoica-Guzun, M. Stroescu, S.I. Jinga, I.M. Jipa, T. Dobre, Ind. Crop. Prod. 50 4746–4752.
(2013) 414–422. [165] C. Legnani, C. Vilani, V. Calil, H. Barud, W. Quirino, C. Achete, S.J.L. Ribeiro,
[116] S.S. Ray, M. Okamoto, Prog. Polym. Sci. 28 (2003) 1539–1641. M. Cremona, Thin Solid Films 517 (2008) 1016–1020.
[117] D. Paul, L.M. Robeson, Polymer 49 (2008) 3187–3204. [166] J. Yang, J. Yu, J. Fan, D. Sun, W. Tang, X. Yang, J. Hazard. Mater. 189 (2011)
[118] S.S. Ray, M. Bousmina, K. Okamoto, Macromol. Mater. Eng. 290 (2005) 759–768. 377–383.
[119] I. Algar, C. Garcia-Astrain, A. Gonzalez, L. Martin, N. Gabilondo, A. Retegi, [167] N. Heßler, D. Klemm, Cellulose 16 (2009) 899–910.
A. Eceiza, J. Renew. Mat. 4 (2016) 57–65. [168] M. Seifert, S. Hesse, V. Kabrelian, D. Klemm, J. Polym. Sci. A Polym. Chem. 42
[120] G.F. Perotti, H.S. Barud, Y. Messaddeq, S.J. Ribeiro, V.R. Constantino, Polymer 52 (2004) 463–470.
(2011) 157–163. [169] O.-A. Saibuatong, M. Phisalaphong, Carbohydr. Polym. 79 (2010) 455–460.
[121] C. Zhijiang, Y. Guang, J. Appl. Polym. Sci. 120 (2011) 2938–2944. [170] S. Gea, E. Bilotti, C. Reynolds, N. Soykeabkeaw, T. Peijs, Mater. Lett. 64 (2010)
[122] S. Saska, L.N. Teixeira, P.T. de Oliveira, A.M.M. Gaspar, S.J.L. Ribeiro, 901–904.
Y. Messaddeq, R. Marchetto, J. Mater. Chem. 22 (2012) 22102–22112. [171] D. Mikkelsen, M.J. Gidley, The Plant Cell Wall: Methods and Protocols, (2011), pp.
[123] H. Luo, G. Xiong, Y. Huang, F. He, Y. Wang, Y. Wan, Mater. Chem. Phys. 110 197–208.
(2008) 193–196. [172] S.-T. Chang, L.-C. Chen, S.-B. Lin, H.-H. Chen, Food Hydrocoll. 27 (2012) 137–144.
[124] M. Ul-Islam, N. Shah, J.H. Ha, J.K. Park, Korean J. Chem. Eng. 28 (2011) [173] Y. Hagiwara, A. Putra, A. Kakugo, H. Furukawa, J.P. Gong, Cellulose 17 (2010)
1736–1743. 93–101.
[125] M. Phisalaphong, N. Jatupaiboon, Carbohydr. Polym. 74 (2008) 482–488. [174] Y. Numata, T. Sakata, H. Furukawa, K. Tajima, Mater. Sci. Eng. C 47 (2015) 57–62.
[126] Z. Cai, P. Chen, H. Jin, J. Kim, Proc. Inst. Mech. Eng. C J. Mech. Eng. Sci. 223 [175] K. Yasuda, J.P. Gong, Y. Katsuyama, A. Nakayama, Y. Tanabe, E. Kondo, M. Ueno,
(2009) 2225–2230. Y. Osada, Biomaterials 26 (2005) 4468–4475.
[127] J. Kim, Z. Cai, H.S. Lee, G.S. Choi, D.H. Lee, C. Jo, J. Polym. Res. 18 (2011) [176] F.G. Torres, O.P. Troncoso, C.G. Grande, D.A. Díaz, Mater. Sci. Eng. C 31 (8)
739–744. (2011) 1737–1740.
[128] W.-C. Lin, C.-C. Lien, H.-J. Yeh, C.-M. Yu, S.-h. Hsu, Carbohydr. Polym. 94 (2013) [177] B. Wei, G. Yang, F. Hong, Carbohydr. Polym. 84 (2011) 533–538.
603–611. [178] H. Bäckdahl, B. Risberg, P. Gatenholm, Mater. Sci. Eng. C 31 (1) (2011) 14–21.
[129] A. Nakayama, A. Kakugo, J.P. Gong, Y. Osada, M. Takai, T. Erata, S. Kawano, Adv. [179] L. Millon, W. Wan, J Biomed Mater Res B Appl Biomater 79 (2006) 245–253.
Funct. Mater. 14 (2004) 1124–1128. [180] L. Fu, J. Zhang, G. Yang, Carbohydr. Polym. 92 (2013) 1432–1442.
[130] Y. Wan, H. Luo, F. He, H. Liang, Y. Huang, X. Li, Compos. Sci. Technol. 69 (2009) [181] W. Czaja, A. Krystynowicz, M. Kawecki, K. Wysota, S. Sakiel, P. Wroblewski,
1212–1217. J. Glik, M. Nowak, S. Bielecki, Cellulose Mol. Struct. Biol. (2007) 307–321.
[131] Y. Dahman, J. Nanosci. Nanotechnol. 9 (2009) 5105–5122. [182] G.F. Picheth, C.L. Pirich, M.R. Sierakowski, M.A. Woehl, C.N. Sakakibara, C.F. de
[132] R.J. Pinto, M.C. Neves, C.P. Neto, T. Trindade, Nanocomposites-New Trends and Souza, A.A. Martin, R. da Silva, R.A. de Freitas, Int. J. Biol. Macromol. 104 (2017)
Developments, InTech, 2012. 97–106.
[133] Y. Zheng, J. Yang, W. Zheng, X. Wang, C. Xiang, L. Tang, W. Zhang, S. Chen, [183] J. Wang, C. Gao, Y. Zhang, Y. Wan, Mater. Sci. Eng. C 30 (2010) 214–218.
H. Wang, Mater. Sci. Eng. C 33 (4) (2013) 2407–2412. [184] Z. Cai, J. Kim, Cellulose 17 (2010) 83–91.
[134] R.J. Moon, A. Martini, J. Nairn, J. Simonsen, J. Youngblood, Chem. Soc. Rev. 40 [185] V. Palaninathan, S. Raveendran, A.K. Rochani, N. Chauhan, Y. Sakamoto, T. Ukai,
(2011) 3941–3994. D.S. Kumar, J. Tissue Eng. Regen. Med. 12 (2018) 1634–1645.
[135] A. Nakagaito, S. Iwamoto, H. Yano, Appl. Phys. A Mater. Sci. Process. 80 (2005) [186] H. Bäckdahl, M. Esguerra, D. Delbro, B. Risberg, P. Gatenholm, J. Tissue Eng.
93–97. Regen. Med. 2 (2008) 320–330.
[136] N. Chiaoprakobkij, N. Sanchavanakit, K. Subbalekha, P. Pavasant, [187] M. Zaborowska, A. Bodin, H. Bäckdahl, J. Popp, A. Goldstein, P. Gatenholm, Acta
M. Phisalaphong, Carbohydr. Polym. 85 (2011) 548–553. Biomater. 6 (2010) 2540–2547.
[137] M.C.I.M. Amin, N. Ahmad, N. Halib, I. Ahmad, Carbohydr. Polym. 88 (2012) [188] N. Bergstrom, S.D. Horn, R.J. Smout, S.A. Bender, M.L. Ferguson, G. Taler,
465–473. A.C. Sauer, S.S. Sharkey, A.C. Voss, J. Am. Geriatr. Soc. 53 (2005) 1721–1729.
[138] J.M. Dugan, J.E. Gough, S.J. Eichhorn, Nanomedicine 8 (2013) 287–298. [189] W. Czaja, A. Krystynowicz, S. Bielecki, R.M. Brown, Biomaterials 27 (2006)
[139] M. Martínez-Sanz, M. Villano, C. Oliveira, M.G. Albuquerque, M. Majone, M. Reis, 145–151.
A. Lopez-Rubio, J.M. Lagaron, New Biotechnol. 31 (2014) 364–376. [190] I. Sulaeva, U. Henniges, T. Rosenau, A. Potthast, Biotechnol. Adv. 33 (2015)
[140] M. Martínez-Sanz, M.A. Abdelwahab, A. Lopez-Rubio, J.M. Lagaron, E. Chiellini, 1547–1571.
T.G. Williams, D.F. Wood, W.J. Orts, S.H. Imam, Eur. Polym. J. 49 (2013) [191] I. Almeida, T. Pereira, N. Silva, F. Gomes, A. Silvestre, C. Freire, J.S. Lobo,
2062–2072. P. Costa, Eur. J. Pharm. Biopharm. 86 (2014) 332–336.
[141] W.-I. Park, M. Kang, H.-S. Kim, H.-J. Jin, Macromol. Symp. 249 (2007) 289–294. [192] N.K. Guimard, N. Gomez, C.E. Schmidt, Prog. Polym. Sci. 32 (2007) 876–921.
[142] K. Tashiro, M. Kobayashi, Polymer 32 (1991) 1516–1526. [193] A. Müller, Z. Ni, N. Hessler, F. Wesarg, F.A. Müller, D. Kralisch, D. Fischer, J.
[143] M. Grunert, W.T. Winter, J. Polym. Environ. 10 (2002) 27–30. Pharm. Sci. 102 (2013) 579–592.
[144] I. Kvien, B.S. Tanem, K. Oksman, Biomacromolecules 6 (2005) 3160–3165. [194] H. Yamamoto, F. Horii, H. Odani, Macromolecules 22 (1989) 4130–4132.
[145] M. Martínez-Sanz, R.T. Olsson, A. Lopez-Rubio, J.M. Lagaron, Cellulose 18 (2011) [195] H. El-Saied, A.H. Basta, R.H. Gobran, Polym.-Plast. Technol. Eng. 43 (2004)
335–347. 797–820.
[146] J.D. Goodrich, W.T. Winter, Polysaccharide materials: performance by design, ACS [196] A. Stoica-Guzun, M. Stroescu, S.L. Jinga, N. Mihalache, A. Botez, C. Matei,
Symp. Ser. (2009) 153–168, https://doi.org/10.1021/bk-2009-1017.fw001. V. Ionita, Int. J. Biol. Macromol. 91 (2016) 1062–1072.
[147] E.E. Brown, M.-P.G. Laborie, J. Zhang, Cellulose 19 (2012) 127–137. [197] S. Chen, Y. Zou, Z. Yan, W. Shen, S. Shi, X. Zhang, H. Wang, J. Hazard. Mater. 161
[148] C. Castro, N. Cordeiro, M. Faria, R. Zuluaga, J.-L. Putaux, I. Filpponen, L. Velez, (2009) 1355–1359.
O.J. Rojas, P. Ganán, Carbohydr. Polym. 126 (2015) 32–39. [198] M. Lu, X.H. Guan, X.H. Xu, D.Z. Wei, Chin. Chem. Lett. 24 (2013) 253–256.
[149] F. Quero, M. Nogi, K.-Y. Lee, G.V. Poel, A. Bismarck, A. Mantalaris, H. Yano, [199] Z. Yang, L. Ren, L. Jin, L. Huang, Y. He, J. Tang, H. Wang, Chem. Eng. J. 344
S.J. Eichhorn, ACS Appl. Mater. Interfaces 3 (2010) 490–499. (2018) 441–452.
[150] L. Yang, H.-Y. Zhang, Q. Yang, D.-N. Lu, J. Appl. Polym. Sci. 126 (2012) [200] T. Oshima, K. Kondo, K. Ohto, K. Inoue, Y. Baba, React. Funct. Polym. 68 (2008)
E245–E251. 376–383.
[151] J.A.A. Ramírez, C.G. Hoyos, S. Arroyo, P. Cerrutti, M.L. Foresti, Carbohydr. Polym. [201] W. Shen, S. Chen, S. Shi, X. Li, X. Zhang, W. Hu, H. Wang, Carbohydr. Polym. 75
153 (2016) 686–695. (2009) 110–114.
[152] S. Goncalves, I.P. Rodrigues, J. Padrão, J.P. Silva, V. Sencadas, S. Lanceros- [202] B.M. Novak, Adv. Mater. 5 (1993) 422–433.
Mendez, L.R. Rodrigues, Colloids Surf. B: Biointerfaces 139 (2016) 1–9. [203] K. Qiu, A.N. Netravali, Polym. Rev. 54 (2014) 598–626.
[153] Q. Lin, Y. Zheng, L. Ren, J. Wu, H. Wang, J. An, W. Fan, J. Appl. Polym. Sci. 131 [204] H. Yano, J. Sugiyama, A.N. Nakagaito, M. Nogi, T. Matsuura, M. Hikita, K. Handa,
(2014) 39848. Adv. Mater. 17 (2005) 153–155.
[154] Y.T. Lin, C.J. Yu, L. Zhu, X.Q. Yin, B.S. Lao, Q. Lin, Applied Mechanics and [205] M. Nogi, S. Ifuku, K. Abe, K. Handa, A.N. Nakagaito, H. Yano, Appl. Phys. Lett. 88
Materials, vol. 320, Trans Tech Publications, 2013, pp. 478–482. (2006) 133124.
[155] J. Qin, Z. Qin, X. Yin, Q. Zeng, L. Zhu, Bioresources 10 (2015) 2185–2194. [206] S. Ifuku, M. Nogi, K. Abe, K. Handa, F. Nakatsubo, H. Yano, Biomacromolecules 8
[156] L. Zhu, J. Qin, X. Yin, L. Ji, Q. Lin, Z. Qin, Polym. Adv. Technol. 25 (2014) (2007) 1973–1978.
168–172. [207] S.C. Fernandes, L. Oliveira, C.S. Freire, A.J. Silvestre, C.P. Neto, A. Gandini,
[157] S.F. Bush, F.G. Torres, J.M. Methven, Compos. A: Appl. Sci. Manuf. 31 (12) (2000) J. Desbriéres, Green Chem. 11 (2009) 2023–2029.
1421–1431. [208] D. Zhang, L. Qi, Chem. Commun. (2005) 2735–2737.
[158] F.G. Torres, S.F. Bush, Compos. A: Appl. Sci. Manuf. 31 (12) (2000) 1289–1294. [209] P. Zhou, H. Wang, J. Yang, J. Tang, D. Sun, W. Tang, Ind. Eng. Chem. Res. 51

1292
F.G. Torres et al. Materials Science & Engineering C 98 (2019) 1277–1293

(2012) 5743–5748. A.C. Pinheiro, A.A. Vicente, L.R. Rodrigues, F. Dourado, Food Hydrocoll. 58
[210] B.R. Saunders, B. Vincent, Adv. Colloid Interf. Sci. 80 (1999) 1–25. (2016) 126–140.
[211] N. Morimoto, T. Ohki, K. Kurita, K. Akiyoshi, Macromol. Rapid Commun. 29 [226] I.M. Jipa, A. Stoica-Guzun, M. Stroescu, LWT Food Sci. Technol. 47 (2012)
(2008) 672–676. 400–406.
[212] K.S. Halake, J. Lee, Carbohydr. Polym. 105 (2014) 184–192. [227] B. Kuswandi, R. Oktaviana, A. Abdullah, L.Y. Heng, Packag. Technol. Sci. 27
[213] L. Wu, H. Zhou, H.-J. Sun, Y. Zhao, X. Yang, S.Z. Cheng, G. Yang, (2014) 69–81.
Biomacromolecules 14 (2013) 1078–1084. [228] B. Kuswandi, A. Restyana, A. Abdullah, L.Y. Heng, M. Ahmad, Food Control 25
[214] W. Hu, S. Chen, B. Zhou, L. Liu, B. Ding, H. Wang, Sensors Actuators B Chem. 159 (2012) 184–189.
(2011) 301–306. [229] B. Kuswandi, C. Maryska, A. Abdullah, L.Y. Heng, J. Food Meas. Charact. 7 (2013)
[215] W. Hu, S. Chen, L. Liu, B. Ding, H. Wang, Sensors Actuators B Chem. 157 (2011) 29–39.
554–559. [230] S. Pourjavaher, H. Almasi, S. Meshkini, S. Pirsa, E. Parandi, Carbohydr. Polym.
[216] W. Wang, T.-J. Zhang, D.-W. Zhang, H.-Y. Li, Y.-R. Ma, L.-M. Qi, Y.-L. Zhou, X.- 156 (2017) 193–201.
X. Zhang, Talanta 84 (2011) 71–77. [231] B.R. Evans, H.M. O'Neill, V.P. Malyvanh, I. Lee, J. Woodward, Biosens.
[217] W. Wang, H.-Y. Li, D.-W. Zhang, J. Jiang, Y.-R. Cui, S. Qiu, Y.-L. Zhou, X.- Bioelectron. 18 (2003) 917–923.
X. Zhang, Electroanalysis 22 (2010) 2543–2550. [232] B. Wang, X. Li, B. Luo, J. Yang, X. Wang, Q. Song, S. Chen, L. Zhi, Small 9 (2013)
[218] M. Phisalaphong, T. Suwanmajo, P. Tammarate, J. Appl. Polym. Sci. 107 (2008) 2399–2404.
3419–3424. [233] H.-W. Liang, Q.-F. Guan, L.-T. Song, H.-B. Yao, X. Lei, H. Yu, NPG Asia Mater. 4
[219] J. He, H. Zhao, X. Li, D. Su, F. Zhang, H. Ji, R. Liu, J. Hazard. Mater. 346 (2018) (2012) e19, https://doi.org/10.1038/am.2012.34.
199–207. [234] S.E. Whitney, M.J. Gidley, S.J. McQueen-Mason, Plant J. 22 (2000) 327–334.
[220] V. Dubey, L.K. Pandey, C. Saxena, J. Membr. Sci. 251 (2005) 131–136. [235] S.E. Whitney, M.G. Gothard, J.T. Mitchell, M.J. Gidley, Plant Physiol. 121 (1999)
[221] S. Cho, N. Almeida, Dietary Fiber and Health, CRC Press, Florida, USA, 2012. 657–664.
[222] S.-B. Lin, L.-C. Chen, H.-H. Chen, J. Food Process Eng. 34 (2011) 1363–1379. [236] H.A. Krässig, Cellulose, structure, accessibility and reactivity, Gordon and Breach
[223] C.-F. Chau, P. Yang, C.-M. Yu, G.-C. Yen, J. Agric. Food Chem. 56 (2008) Science Publishers, Philadelphia, USA, 1993.
2291–2295. [237] F.G. Torres, O.P. Troncoso, D. Lopez, C. Grande, C.M. Gomez, Soft Matter 5 (2009)
[224] A. Okiyama, M. Motoki, S. Yamanaka, Food Hydrocoll. 6 (1993) 503–511. 4185–4190.
[225] J. Padrao, S. Gonçalves, J.P. Silva, V. Sencadas, S. Lanceros-Méndez,

1293