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Transcript of Recent advances in bacterial cellulose
REVIEW PAPER
Recent advances in bacterial cellulose
Yang Huang • Chunlin Zhu • Jiazhi Yang •
Ying Nie • Chuntao Chen • Dongping Sun
Received: 12 July 2013 / Accepted: 14 October 2013 / Published online: 27 October 2013
� Springer Science+Business Media Dordrecht 2013
Abstract Bacterial cellulose (BC) produced by
some microorganisms has been widely accepted as a
multifunctional nano-biomaterial. It is composed of
linear glucan molecules attached with hydrogen
bonds, which appears similar to plant cellulose.
However, when compared with other conventional
natural or synthesized counterparts, BC performs
better in areas such as biomedicine, functional
devices, water treatment, nanofillers, etc. for its
distinct superior chemical purity, crystallinity, bio-
compatibility, and ultrafine network architecture.
When BC is incorporated in a material or used as a
scaffold, novel features result that are related to BC’s
intrinsic characteristics mentioned above. This review
mainly summarizes the recent developments of the
functional products fabricated with BC. Besides, the
controllable cultivation conditions should also be
discussed for expecting to make a breakthrough in
its productivity. We highlight the literatures mainly in
last 5 years, exerting ourselves to provide the state-of-
the-art opinions in areas wherever are focused on for
BC researching.
Keywords Bacterial cellulose � Nano-
biomaterials � Network architecture �Controllable cultivation
Introduction
Cellulose synthesized by plants or bacteria is an
almost inexhaustible organic polymer resource on
Earth and has global economic importance (Kim et al.
2006). By estimation, the amount of cellulose synthe-
sized globally each year is between 100 and 150
billion tons (Hon 1994). Thus, cellulose is expected to
meet the increasing demand for environment friendly
and petroleum-replacing products. These natural
polymers have been conventionally used in a wide
range of fields such as papermaking (Saikia et al.
1997), textile industry (Perepelkin et al. 1997),
medical applications (Hoenich 2007), reinforcement
agent (Bhatnagar and Sain 2005; Wu et al. 2007), etc.
for their good biocompatibility, high rigidity, fibrous
morphology and low cost.
Recently, a special natural cellulose, i.e. bacterial
cellulose (BC) has gained particular interest. BC
synthesized by certain bacteria, such as Acetobacter
xylinum, was initially reported by Brown in (1886). It
is hypothesized that bacteria produce cellulose for the
protection from ultraviolet radiation and harsh chem-
ical environment and access to oxygen (Brown 2004;
Eichhorn et al. 2001; Iguchi et al. 2000; Klemm et al.
2005; Putra et al. 2008; Retegi et al. 2010; Shoda and
Y. Huang � C. Zhu � J. Yang � Y. Nie �C. Chen � D. Sun (&)
Chemicobiology and Functional Materials Institute,
School of Chemical Engineering, Nanjing University of
Science and Technology, Nanjing 210094,
People’s Republic of China
e-mail: [email protected]
123
Cellulose (2014) 21:1–30
DOI 10.1007/s10570-013-0088-z
Sugano 2005; Somerville 2006), while plant cell wall
made of cellulose provides support against osmotic
pressure. As the cellulose derived either from plants or
bacteria is biocompatible and biodegradable, it is the
potential to be used in biomedical fields.
Though the chemical constitution of BC is the chain
molecules linked by cellobiose, as same as other
cellulose, it is free of contaminant molecules, such as
lignin, hemicelluloses, and pectin, etc., which are
normally found in plant-derived cellulose. The per-
centage of cellulose content in cotton is 90, and 50 %
in wood due to some amorphous polymers that are also
embedded such as neutral and acidic polysaccharides,
glycoproteins, and waxy aromatic substances (Conner
1995). Thus BC can be easily purified with NaOH
solution with low energy consumed. Therefore, BC’s
chemical purity can also be maximally maintained
without the use of other chemicals (Sani and Dahman
2010). The degree of polymerization (DP) of BC is
ranging from 300 to 10,000 depending on the culti-
vation conditions, various additives, and finally the
bacterial strains (Vitta and Thiruvengadam 2012).
Unlike plant cellulose, BC produced from micro-
organisms has a unique mechanism in the synthesis of
chain molecules followed by a subtle self-assembly
progress. A single A. xylinum cell may polymerize up
to 200,000 glucose molecules per second (Hestrin and
Schramm 1954) with cellulose synthase or terminal
complexes (TC) presented in pores on the cell surface
and then extruded into the surrounding medium,
typically achieve the form of a ribbonlike bundles
with length from 1 to 9 lm. The details of the process
are described below and illustrated in Fig. 1.
Micrographs of the surface of the cell envelope
indicate the presence of some 50–80 porelike sites
arranged in a regular row along the longitude of the cell
and in evident juxtaposition with the extracellular
cellulosic ribbon (Brown et al. 1976; Zaar 1979). These
discrete structures of the lipopolysaccharide layer are
presumed to be the sites of extrusion for precellulosic
polymers in groups of ca. 10–15 chains to associate with
each other forming the so-called subfibrils with a width
of 1.5 nm (Ross et al. 1991). These subfibrils are then
self-assembled to form microfibrils, and then a fibrillar
ribbon is formed followed by their side by side tightly
aggregation with width ca. 50–80 nm, which are 200
times finer than cotton fibers and exhibit an extraordi-
nary high surface area (Vitta and Thiruvengadam 2012).
The spatial arrangement of the pre-microfibril aggre-
gation provides a high crystallinity up to 84–89 %
Fig. 1 The details arrangement of fibrils extruded from cell surface and their self-assembly process
2 Cellulose (2014) 21:1–30
123
(Czaja et al. 2004), while the data varies from 40 to 60 %
for plant cellulose (Jonas and Farah 1998). It results to a
typical Young’s modulus of BC in the range 15–35 GPa,
with the tensile strength in the range 200–300 MPa
(Brown et al. 1976). The relative high modulus makes it
act as reinforcing elements in polymer matrix. The
crystal structures of crystalline cellulose existed in the
cellulose derived from different resources are also
different in terms of two different crystalline phases: Iaand Ib that are corresponding respectively to triclinic and
monoclinic unit cells (Atalla and Vanderhart 1984). It
has been reported that most plant cellulose is Ib-rich,
while BC is found to be Ia-rich (Sugiyama et al. 1985),
and the proportion of cellulose Ia exceeds 80 % (Sun
et al. 2007). The crystal structure is one of the most
important factors influencing on the mechanical and
interfacial properties of the cellulose (Nishiyama et al.
2002).
BC produced in the static cultivation method seems
to be a hydrogel sheet with a three-dimensional (3D)
reticulated network structure which could be observed
under microscope (Fig. 2). The obtained never-dried
sheet has about 100 times higher in ratio between wet
and dry weight. The extremely high water content was
attributed to the native hydrophilicity of cellulose as
well as the presence of pore structure and ‘‘tunnels’’
within the wet pellicle which result in the extensive
interior surface area of the interstitial spaces of the
never dried matrix (White et al. 1989). Due to BC has
unique nanofibril network morphology which mimics,
to some extent, properties of the extracellular matrix,
it has the potential to act as a scaffold for tissue
engineering. Besides the applications in biomedical
areas, dried BC membrane has also been used as
diaphragms for loudspeakers (Iguchi et al. 2000), food
packaging films (Wanichapichart et al. 2012), and
vulnerable historic silk fabrics reinforcement for
storage and display (Wu et al. 2012). More recently,
some new areas have been focused on in order to
develop the distinctive features further of this novel
biomaterial. The integration of optical activity (Hu
et al. 2011d), electrical conductivity (Hu et al. 2011b),
magnetic nanoparticles (Zhang et al. 2011a), or
photocatalytic degradation (Zhang et al. 2011b)
materials to cellulosic matrix for certain applications
has been a hot research field in the last decades.
After all, a wider application of this promising
polysaccharide polymer apparently depends on the
practical considerations such as the scale-up capability
and production costs, so factors during its cultivation
for achieving large-scale industrial production includ-
ing carbon and nitrogen sources and bacterial species
and even fermentation instruments should also be
investigated.
BC fermentation
For improving the BC production, many species of
bacteria can be listed as the candidates such as those in
the genera Gluconacetobacter (formerly Acetobac-
ter), Agrobacterium, Aerobacter, Achromobacter,
Alcaligenes, Azotobacter, Rhizobium, Sarcina, Sal-
monella, Escherichia, etc. The metabolic products (i.e.
BC) may go through different routes before secreting
outside of cells. Therefore, scientific significance
could be found when dealing with different strains or
studying one strain with a mutation method. The
Fig. 2 BC produced in static cultivation (a) and SEM image of BC (b)
Cellulose (2014) 21:1–30 3
123
essential nutrients as well as fermentation style will
also affect the output of BC significantly.
Screening and mutating strain for BC production
In 2001, Fujiwara et al. (2001) reported a bacterial
strain Enterobacter sp. producing bacterial cellulose
for the first time. After that, Zogaj et al. (2003) isolated
a strain from human gut and recently, Hungund and
Gupta (2010a) tried to improve its cellulose produc-
tion by investigating effects from various of carbon
sources, nitrogen sources and other factors on the
metabolism path of Enterobacter amnigenus GH-1
isolated from a rotten apple.
The pellicle at the air–liquid interface during
production of grape wine initially found as a contam-
inant was ultimately proved to be BC. Rani et al.
(2011) attempted to isolate the bacterium which is
responsible for the pellicle production. At last the
bacterium was obtained and identified as Glu-
conacetobacter sp. The yield of BC in grape extract
was found to be 7.47 g/L as dry weight after 2 weeks
of incubation under stationary condition at ambient
temperature. And in HS medium it was found to be
only 1.76 g/L. The results indicate that the bacterium
prefer grape medium to HS broth for higher produc-
tion of BC, but the specific reason is still not clear.
Though strain mutagenesis is an effective approach
to increase BC productivity, few publications about
that has been reported. Ishikawa et al. (1995) obtained
mutants of A. xylinum BPR 2001 resistant to sulfa-
guanidine by NTG (N-methyl-N/-nitro-N-nitrosogua-
nidine) treatment. Bapiraju et al. (2005) reported
mutation induced enhancement of lipase production
from Rhizopus sp. using UV radiation and NTG.
Kadam et al. (2006) successfully employed UV
mutagenesis to optimize strain of Lactobacillus del-
bruekii for lactic acid production. Hungund and Gupta
(2010b) reported strain improvement of Glu-
conacetobacter xylinus using UV radiation and ethyl
methanesulfonate (EMS). The mutant GHEM4 has a
cellulose yield of 5.96 g/L which was 50 % more than
the parental strain (GHUV4) and 98 % more than that
of wild strain (NCIM 2526). Effectiveness of UV
radiation (physical mutagen) and EMS (chemical
mutagen) in strain improvement for enhanced cellu-
lose production has been demonstrated.
However, since these mutagenesis methods have
radiation or toxicity which is rather harmful to human
health, their applications are limited. It is meaningful
to find new mutagenic treatments to increase BC yield
of BC-producing bacteria. Wu et al. (2010) increased
the BC yield with a Gluconoacetobacter xylinus strain
through mutagenesis induced by high hydrostatic
pressure (HHP) treatment. The parental strain in its
exponential phase was treated at 250 MPa and 25 �C
for 15 min to induce mutagenesis using a HHP
machine (Fig. 3). Among the mutants, strain M438
showed the highest BC hygrometric state yield
(158.56 g/L in average for five generations) and the
lowest coefficient of variation (2.4 % for five gener-
ations). Thus, HHP treatment can serve as an effective
method to cause mutagenesis with high BC-producing
ability. And then, Ge et al. (2011) studied the genetic
diversity of strain M438 and its initial strain by
amplified fragment length polymorphism. The results
indicated that strain M438 was a deletion mutant
induced by HHP, and the only deleted sequence
showed 99 % identity with 24,917–24,723 bp in the
genome sequence of Ga. Hansenii ATCC23769,
and the complement gene sequence was at
Fig. 3 Mechanical construction of the HHP equipment: 1 top
cover, 2 treatment room, 3 high pressure cylinder, 4 temperature
control system, 5 high pressure piston, 6 low pressure piston, 7
low pressure cylinder, and 8 hydraulic compress or with
automatic control system. The treatment pressure and treatment
time can be automatically controlled by the hydraulic compres-
sor, with tailor-made castor oil as pressure transmitting medium.
The treatment temperature can be kept constant by the
temperature control system (Reprinted from Wu et al. 2010
with permission from Springer)
4 Cellulose (2014) 21:1–30
123
24,699–25,019 bp with local tag GXY_15142, which
codes small multi drug resistance (SMR) protein.
Therefore, the author believed SMR might be the
inhibitory actions for BC producing.
FE-SEM images of the cellulose product after
purification and freeze-drying are presented in Fig. 4
(Kumagai et al. 2011). The width of cellulose fibrils in
A. bogorensis AJ strain and G. xylinus is ranging from
5 to 20 nm and from 40 to 100 nm, respectively,
suggesting differences in the mechanism of cellulose
biosynthesis or organization of cellulose synthesizing
sites in these two related bacterial species. It is
important to find reasons for the differences in the
quantity and morphology of cellulose produced by A.
bogorensis and G. xylinus. And this will in contrast
provide a better understanding of the mechanism of
cellulose biosynthesis.
Carbon and nitrogen sources on cellulose
production
In recent years, various carbon sources including
monosaccharides, oligosaccharides, alcohols, sugaral
cohols and organic acids, have been used to maximize
bacterial cellulose production by various G. xylinus
strains (Ishihara et al. 2002; Keshk and Sameshima
2005; Masaoka et al. 1993; Matsuoka et al. 1996;
Mikkelsen et al. 2009; Yang et al. 1998). G. xylinus has
two main operative amphibolic pathways (Fig. 5): the
pentose phosphate cycle for the oxidation of carbohy-
drates and the Kreb scycle for the oxidation of organic
acids and related compounds (Bielecki et al. 2005; Ha
et al. 2011; Ross et al. 1991; Sutherland 2001).
In order to determine the effects of various culture
conditions, initial screening with various carbon
sources (2 %) including monosaccharides, disaccha-
rides and polysaccharides was carried out using HS
medium as the base. Organic and inorganic nitrogen
sources were also studied (Rani and Appaiah 2011)
(Table 1).
The results shown from Table 1 indicate that,
glucose seems to be the best carbon source. It
demonstrates the validity of the results that various
carbon substrates could be converted to monomer
glucose by Gluconacetobacter, followed by polymer-
ization to BC (Mikkelsen et al. 2009). When various
nitrogen sources were added to the HS medium,
peptone is found to be the most effective nutrient.
However, corn steep liquor which produced the
second highest production is always chosen as a
substitution for the economic viewpoints. Obviously,
inorganic nitrogen could not act as the preferable
choice for their general low BC productivity.
In recent years, many studies have been focused on
attempts to produce BC by using alternative feed
stocks, such as food processing effluents, hemicellu-
loses in waste liquor from atmospheric acetic acid
pulping, molasses, konjak glucomannan, fruitjuice,
ricebark, black strap molasses solution, and wheat
straw (Carreira et al. 2011; El-Saied et al. 2008; Hong
et al. 2011; Kongruang 2008; Kurosumi et al. 2009).
These raw materials are abundant and either industrial/
agricultural waste or relatively inexpensive agricul-
tural products. This strategy could not only reduce
burden on environment but also achieve the goal of
large scale production with low cost.
Fig. 4 FE-SEM images of the cellulose pellicle produced by A. bogorensis (a) and G. xylinus (b) (Reprinted from Kumagai et al. 2011
with permission from American Chemical Society)
Cellulose (2014) 21:1–30 5
123
BC production in bioreacter
BC is produced as the pellicle type on the surface of
the medium under static culture conditions. However,
the traditional static culture method cannot be applied
for mass production, as it requires a long culture
period and intensive labor and results in low produc-
tivity (Chao et al. 2000). Therefore, it is infeasible for
large scale industrial production. For a higher BC
yield, low shearing force and high oxygen transferrate
are necessary in an agitate fermentation pattern with
certain strain.
Song et al. (2009) developed a method for the mass
production of BC, using a spherical type bubble
column bioreactor (Fig. 6) modified from an airlift-
type reactor. The spherical type bubble column
bioreactor with low shear and high oxygen transfer
rates could reduce cel- mutant bacteria and thus
improved the BC yield. The optimum aeration rate
was determined 1.2 vvm (6 L/min) by measuring the
kLa in a 10 L spherical type bubble column bioreactor.
The yield of BC reached to 5.6 and 5.8 g/L using
saccharified food wastes with the addition of 0.4 %
agar in the 50 and 10 L spherical type bioreactor,
respectively. And Choi et al. (2009) investigated the
productivity and physical properties of BC produced
with various different methods, such as the static
culture and the modified bubble column culture using
a 10 and 50 L spherical airlift-type bioreactor.
Different types of plastic composite support (PCS)
(Fig. 7) were implemented separately within a fer-
mentation medium in order to enhance BC production
by Cheng et al. (2009). The highest BC yield was
7.05 g/L in one of the PCS biofilm reactors mentioned
above. Later, Cheng et al. (2011) added carboxy-
methyl cellulose (CMC), a soluble form of cellulose,
previously reported to enhance BC production in
pellet form, to the BC-producing medium with the
Fig. 5 Proposed biochemical pathways for the production of BC (Reprinted from Ha et al. 2011 with permission from Elsevier)
6 Cellulose (2014) 21:1–30
123
implementation of PCS biofilm reactor. The BC pro-
duction was improved to the maximum (*13 g/L)
when 1.5 % of CMC was applied.
BC application in medical field
Bacterial cellulose (BC) synthesized from A. xylinum
has drawn more and more attention and interest in the
field of biomedical device due to its unique structure
and properties. Characteristics, such as relatively high
tensile strength, extremely hydrophilic surface,
homologous structure with native extracellular matrix,
unique nanostructure and excellent biodegradability
and biological affinity etc. make BC as a promising
material in biomedical applications.
Table 1 Screening of carbon and nitrogen sources for pro-
duction of BC (Reprinted from Rani and Appaiah 2011 with
permission from Springer)
Carbon source (2 %, w/v) BC (%) pH
Glucose 100a 4.36
Glycerol 85.51 4.19
Sucrose 77.03 4.57
Fructose 73.49 4.58
Pectin 33.21 4.03
Arabinose 19.08 3.97
Cellobiose 16.96 4.49
Sorbitol 15.90 4.62
Galactose 15.54 4.18
Trehalose 15.19 4.52
Xylose 14.84 3.88
Rhamnose 14.13 4.62
Maltose 13.42 4.45
Starch 9.18 4.66
Mannose 5.30 4.08
Organic nitrogen source (2 %, w/v)
Yeast extract 37.28 4.63
Peptone 100a 3.51
Tryptone 0 3.09
Beef extract 57.20 3.94
Corn steep liquor 77.54 4.77
Inorganic nitrogen source (1 %, w/v)
Sodium nitrate 0 3.11
Ammonium nitrate 0 2.99
Ammonium sulphate 8.05 4.29
Ammonium acetate 4.66 5.75
a Yield from glucose and peptone 2 % taken as 100 %
Fig. 6 Apparatus of 50L spherical type bubble column
bioreactor. 1 Nozzle for inoculation; 2 Steam manometer; 3
Air outflow; 4 Nozzle for injection; 5. Thermometer; 6 A
transfer pump; 7 DO electrode; 8 pH electrode; 9 Water jacket;
10 Water jacket (inflow/outflow); 11 Air inlet; 12 Sampling
nozzle; 13 Air filter; 14 Control box of acid and alkali inlet; 15
Acid storehouse; 16 Alkali storehouse; 17 A constant-temper-
ature water bath; 18 Steam boiler; 19 Compressor; 20 Air flow
meter (Reprinted from Song et al. 2009 with permission from
Springer)
Fig. 7 Plastic composite support (PCS) tubes bound to agitator
shaft and bioreactor design (Reprinted from Cheng et al. 2011
with permission from American Chemical Society)
Cellulose (2014) 21:1–30 7
123
Wound-dressing materials
The goals of wound healing are to recover the
biological and structural function of the skin and to
block scar tissue formations. BC seems to be a suitable
substitute for human skin to create a protective barrier
as well as to deliver therapeutic compounds during the
wound-healing. Besides the criteria mentioned above,
there should be specific requirement for the desired
wound healing material.
Antimicrobial activity
First of all, the material should have antimicrobial
activity and can provide a barrier against wound
infection, which is a major factor to all wound care
procedures. BC nanofibers were used as a template for
the precipitation of silver (Ag) nanoparticles via in situ
liquid phase redox reaction between AgNO3 and
NaBH4. Ag nanoparticles with an average diameter of
1.5 nm were homogeneously spreaded on BC. Good
dispersion and nano-dimension provide Ag particles
an extremely developed specific surface, and conse-
quently guarantees the hybrid nanofibers an efficient
antimicrobial property. The colony-counting method
was conducted to investigate the antimicrobial activity
against E. coli and the reduction in bacteria for the Ag/
BC nanofibers was 99.2 % (Yang et al. 2011b). Cai
et al. (2011a) prepared the antimicrobial material in
the same way, but with an ultrasound procedure to
make Ag? penetrate into BC matrix more easily, and
as a result, the silver nanoparticles homogeneously
distributed and the amount of loading on the fibers is
also improved.
Wei et al. (2011) immersed the freeze-dried BC
film in a benzalkonium chloride solution, a cationic
surfactant type antimicrobial agent, followed by
another freeze-drying step. A stable and lasting release
of the antimicrobial agent within at least 24 h was
achieved by the prepared BC dry film, which could
afford nice permanence of the antimicrobial activity as
wound dressing.
Nanofibril network morphology
The biomedical applications of bacterial cellulose
(BC) as a dressing material are mainly dependent on
its water holding capacity (WHC) and water release
rate (WRR), which in turn depend on pore size, pore
volume and surface area (Ul-Islam et al. 2012).
As known to all, the cell-substrate interaction is
quite important in the area of tissue engineering. The
topographical of the extracellular matrix (ECM)
usually have a significant effect on cellular behavior.
Generally speaking, tissue development is controlled
in three matrix size scales. The gross shape and size of
tissue is decided by the macroscope shape (cm to mm
scale) of matrix; cell invasion and growth is controlled
by the size and structure of the matrix pore (lm); the
adhesion and gene expression of cells are adjusted by
the surface chemistry of the matrices (nm scale). Thus,
the pore size of porous substrates used in tissue
engineering has important effects on cell behavior
(Rambo et al. 2008; Cai et al. 2011b). Besides, certain
porosity is also necessary for transferring the air and
substrate onto the skin, retaining executes effectively
(Sun et al. 2011), and achieving a moist environment
to reduce wound pain.
Backdahl et al. (2008) constructed a microporous
BC scaffold by culturing A. xylinum together with
porogen materials of starch and paraffin. Porogens
could be removed with several cleaning steps. Smooth
muscle cells could migrate into the material to a
greater extent than into a pellicle produced in a static
culture. Rambo et al. (2008) cultivated BC membranes
with pin templates, allowing the bacteria to synthesize
cellulose fibers around the pins, and as a result forming
a porous membrane with pore diameters varying from
60 to 300 lm. The obtained micropore membrane
could avoid wound contraction owing to the porous
substrate effects towards prothetic cell behavior. Gao
et al. (2011b) prepared BC sponges (Fig. 8) via
emulsion freeze-drying technique in order to possess
the large pores and nanopores with a high surface area
and a high porosity. The BC sponges also exhibit
excellent cell compatibility as fibrous synovium-
derived mesenchymal stem cells (MSCs) could pro-
liferate well on and inside the matrix.
Artificial skin
Thanks to its unique network structure, high water
content, and mechanical characteristics, BC could
potentially be used not just as a wound healing
treatment, but as a semipermanent artificial skin and
induce epithelial recovery even after the severest
epithelial damage. A cell-seeded BC skin substitute
8 Cellulose (2014) 21:1–30
123
could be an improved alternative to autografting for
patients with severe skin damage (e.g. burn victims,
Stevens-Johnson syndrome, etc.) (Petersen and Gaten-
holm 2011). Lin et al. (2011) fabricated a macroporous
BC hydrogel via physical destruction, sequential
modification with different ECM (collagen, elastin
and hyaluronan), and growth factors (B-FGF, H-EGF,
and KGF) as a strategy to enhance its biodegradability
and biocompatibility. As a result, modifying BC
hydrogel with collagen or growth factors H-EGF
may be a feasible method to improve the biocompat-
ibility and thus provide highly desirable characteris-
tics for ideal skin substitutes.
Vascular tissue engineering
The emergence and increase of coronary heart
diseases (Rosamond et al. 2008) brings about the need
of replacement blood vessels. Synthetic blood vessels,
such as polyethylene terephthalate (PET), or Dacron,
and expanded polytetrafluorethylene (ePTFE) are the
most common vascular graft materials for lower-
extremity bypass surgery, but have satisfactory suc-
cess only with large-diameter vessels while their
performance is poor as small-diameter vessels those
with diameter \ 6 mm due to early thrombosis (Fink
et al. 2011; Rosamond et al. 2008). To date, the search
for a suitable artificial small-diameter blood vessels is
still ongoing since nothing has yet immerged to give a
satisfactory long-term success (Hamilton and Vorp
2004).
However, BC as a promising material in biomedical
applications seems to have some advantages over the
synthetic polymer mentioned above. (1) Using special
production techniques, BC can be shaped into tubes of
practically any lengths and diameters (Bodin et al.
2007b). (2) The compliance and mechanical properties
of BC resembles that of native arteries (Backdahl et al.
2006). (3) Naked BC tubes are biocompatible, and
show good blood compatibility when tested in vitro
and in vivo (Esguerra et al. 2010; Fink et al. 2010;
Helenius et al. 2006). (4) The inner surface of a BC
graft can be modified to further increase blood
compatibility (Bodin et al. 2007a). (5) and the porosity
of the BC scaffold can be altered to facilitate cell
ingrowth (Rosamond et al. 2008).
The tubular BC gel with a desired length, inner
diameter, and thickness (Fig. 9) has been synthesized
by a simple technique in a short cultivation time (Putra
et al. 2008). The growth of a BC tube in a vertical
Fig. 8 Photos of side views of a columned BC sponge, b cuboid BC sponge and top views of c columned BC sponge, d cuboid BC
sponge (Reprinted from Gao et al. 2011b with permission from Springer)
Cellulose (2014) 21:1–30 9
123
fermentation bioreactor using silicone tubing for
support and as an oxygen delivery membrane has also
been researched by Backdahl H and his coworkers.
The tubular-shaped bacterial cellulose (BC-TS) could
be used as a blood vessel replacement (Backdahl et al.
2011; Klemm et al. 2001). The produced dense, thin
layers of BC network give the resulting tubes good
mechanical properties. These BC tubes have been
tested in a pig model as an infrarenal aortic bypass and
show promising results for using as vascular grafts in
the future.
Mechanical properties
Although BC has superior strength and stability in the
wet state (Astley et al. 2003; Nakayama et al. 2004)
like native blood vessels, it has poor elasticity
(Backdahl et al. 2006). Fibrin on the other hand, has
remarkable elasticity, reaching up to a maximum of
330 % extensibility (Liu et al. 2006), but insufficient
strength when subjected to physiological environ-
ments (Jockenhoevel et al. 2001; Shaikh et al. 2008).
Mechanical properties of real blood vessel (BV) are
attributed to its composite structure of rubbery and
stiff fibrous constituents (Shadwick 1999). Thus a
similar composite structure can be envisioned to
develop a suitable replacement material. Brown
fabricated the BC/fibrin composites by immersing
the never-dried BC sheets in the fibrin solution with
the glutaraldehyde as a crosslinker. As estimated, BC/
fibrin composites display significantly higher strength
and elongation over native BC. The result from
mechanical measurement illustrated that the compos-
ites had ultimate tensile strength, modulus and time-
dependent viscoelastic properties comparable to those
of a native small-diameter blood vessel (Brown et al.
2012).
Anticoagulant character
Biocompatibility refers to the ability of a biomaterial
to perform with an appropriate host response in a
specific situation (Williams 1987). It is well known
that, blood-contacting biomaterials and artificial
organs, such as artificial blood vessels, pumps and
artificial hearts, require improved blood compatibility
for clinical use. However, vascular substitutes avail-
able currently (e.g. Polyurethane, Dacron, and ePTFE)
still can not fully achieve the goal. Vascular graft
failure is mainly caused by thrombosis/thromboem-
bolism and intimal fibrous hyperplasia (Padera and
Schoen 2004).
Fink et al. (2010) firstly evaluated the thrombogenic
properties of vascular graft tubes based on BC, compar-
ing it with commercial vascular grafts of poly(ethylene
terephtalate) (PET) and expanded poly(tetrafluoroethyl-
ene) (ePTFE). The results showed that BC does not
induce plasma coagulation to any great extent. In
comparison with PET and ePTFE shown in Fig. 10,
BC performed very well and was found to induce the
least and slowest activation of the coagulation cascade.
Wan et al. (2011a) prepared a novel class of
nanofibrous scaffold for vascular tissue engineering by
hybridizing heparin and bacterial cellulose for pre-
venting the formation of blood clot. Heparin has been
widely used for the surface modification of various
biomaterials related to vascular use (Linhardt et al.
2008; Oliveira et al. 2003), because it is an anticoag-
ulant that prevents thrombus. In another way, Andrade
et al. (2010, 2011) attempted to modify BC surface
with the tripeptide Arg-Gly-Asp (RGD) which could
act as an adhesive between BC and endothelial cells.
Almost no platelets were adhered when endothelial
cells were cultured simultaneously. In contrast, BC
seeded with endothelial cells, which mimicks the
native vessel, would obviously improve its blood
compatibility.
Fig. 9 The BC-TS gels cultured in the silicone tubes of various
inner diameters: a–f lateral view of BC-TS with an outer
diameter of 20, 10, 5, 4, 3, and 1 mm, respectively, and g top
view of BC-TS with an outer diameter of 10 mm (Reprinted
from Putra et al. 2008 with permission from Elsevier)
10 Cellulose (2014) 21:1–30
123
Bone tissue regeneration
Bone is made of a matrix comprised largely of
collagen which is mineralized by hydroxyapatite. This
results in stiffness and strength to the composite. As
Webster and Ahn described, bone can be viewed as a
hierarchical nanostructure biomaterial, starting from
the smallest collagen molecules (1 nm in diameter)
connected with apatite nanocrystals (5 nm in diame-
ter) to the ends, forming mineralized collagen nanof-
ibers (50 nm in width) first, then fiber bundles, bone
lamella (3–7 lm), bone osteons (10–500 lm), finally
bone (Webster and Ahn 2007). A synergistic scaffold
has been developed in order to mimic this hierarchical
structure of bone (Wang and Yu 2010). As one of the
most popular biomemetic approaches for bone tissue
engineering, electrospun nanofibers made of synthetic
polymers have been intensively investigated as bio-
materials for bone regeneration (Jang et al. 2009).
However, nanofiber itself cannot fulfill the mechanical
strength requirement for bone; thus, it has to be
applied with the strong substrate materials (Wang
et al. 2010).
As mentioned above, bone tissue is mainly com-
posed of hydroxyapatite (HAp) and collagen. BC is an
attractive alternative to mimic collagen fibers because
of its biocompatibility, high tensile strength in dry and
wet states, fine fibril network, high crystallinity, and
moldability. As a result, BC has been focused on using
as a potential bone tissue scaffold for its nanostructure
and morphological similarities with collagen which
could act as a matrix for providing maximum integra-
tion with cells and body fluids. In addition, BC also has
a nanostructure surface which facilitates the adhesion
of cells.
HAp has been extensively investigated in bone
regeneration and becomes a substitute for bone and
teeth regeneration because of its excellent biocom-
patibility, non-inflammatory, non-toxic, non-immu-
nogenic and bioactivity, especially the nanoscale HAp
(Liao et al. 2003). To imitate the sedimentation and
growth of HAp crystals on collagen fibrils surface,
simulated body fluid (SBF) solution is a common
method for fabricating the BC/HAp composites.
However, owing to that the hydroxyl group exposed
out of cellulose does not have enough activity to
Fig. 10 Representative time-lapse images from imaging of
coagulation tests in PFP at the exposed lumen of PET, ePTFE
and BC graft samples. Graft material samples are attached along
the left wall in the images. The colour represents the density of
the formed fibrin network. PET demonstrates a fast activation of
the coagulation process while BC demonstrates an intermediate
activation and ePTFE only activates coagulation modestly.
From the images it seems that propagation of coagulation from
the surface is faster from both PET and ePTFE graft samples
than from the BC sample. (Reprinted from Fink et al. 2010 with
permission from Elsevier)
Cellulose (2014) 21:1–30 11
123
absorb Ca2? at the initial stage, surface modification
of cellulose before mineralization should be con-
ducted in advance.
Surface modification for mineralization
Gao et al. (2011a) introduced the e-polylysine (PLL), a
natural coming peptide, to the surfaces of BC nanof-
ibers via crosslinking method by using procyanidins as
crosslinker. The bioactivity of BC nanofibers coated
with PLL was demonstrated by the bone-like HAp
deposition throughout the scaffold in a simulated body
fluid (SBF). When BC/PLL was immersed in CaCl2solution, Ca2? was absorbed quickly onto the surface
of the fibers by electrostatic interactions between Ca2?
and –COOH of PLL. Subsequently, CO32- and PO4
3-
in the SBF rapidly combined with Ca2? attached on
the BC/PLL nanofibers to form the nuclei of HAp. The
nuclei then underwent a mineralization process to
generate low crystallinity, platelet-like carbonated
HAp along the PLL-BC fibers and finally the miner-
alized BC/PLL nanocomposites were obtained which
were very similar to the architecture and composition
of natural bone.
Yin et al. (2011a) prepared the nanocomposites by
the adsorption of polyvinylpyrrolidone (PVP) to
initiate the nucleation of HAp and Wang et al.
(2011a) replaced it with the cost-effective gelatin
and furthermore a better cell-binding properties were
obtained. Wan et al. (2011b) also confirmed the
increased amount of COOH group on the carbon
nanofibers after oxidized in nitric acid.
As the fluorescence microscopy analysis demon-
strated that osteoprogenitor cells preferred adhesion to
mineralized BC over pure BC scaffolds (Fig. 11)
(Zimmermann et al. 2011), and nano-otholits regarded
as an osteoinductor, stimulate bone regeneration and
enable bigger migration of the osteoblasts for the
formation of the bone tissue when coupled with
collagen and BC membranes. The biomaterial pre-
sented in the ear internal bony fishes, is constituted of
some elements that are constituents of the bones, such
as collagen (protein) and otoliths together with a
gelatinous matrix and calcium carbonate. As a result,
higher osteoblast activity can be observed in the
histological experiment (de Olyveira et al. 2011).
Other applications in medical field
Mohd Amin et al. (2012) prepared the hydrogels for
drug delivery with powdered BC and acrylic acid by
exposure to accelerated electron-beam irradiation.
Results suggested that the hydrogels were both
thermo- and pH-responsive thus made it a candidate
in a controlled delivery system for protein based drugs.
Cellulose fabricated together with micro-channels
(Ø * 500 lm) in order to mimic the ultrastructure
of the central region of the knee meniscus. Results
showed that the micro-channels could facilitate the
alignment of cells and collagen fibers, and the parallel
orientation of collagen fibers in contrast strengthen the
tissues, making it suitable for knee menisci and
tendons replacement (Martınez et al. 2012). Recouv-
reux et al. (2011) synthesized the large, organ-like
Fig. 11 Fluorescent microscopy images (blue stain nucleus, red stain actin): a pure BC control scaffold and b mineralized BC scaffold
(Reprinted from Zimmermann et al. 2011 with permission from Elsevier)
12 Cellulose (2014) 21:1–30
123
three-dimensional BC hydrogels with the potential
applications in implantable tissue and organ scaffolds
such as kidney or liver. Tests in structural character-
istics, mechanical properties and biocompatibility are
all carried out and a superior performance could be
totally expected. Also, a sponge prepared by cross-
linking blended BC and sodium alginate solution
following with the freeze-drying process has been
developed for the use as mucosal flaps in oral tissue
regeneration. The composites with 30 % alginate have
advantages in terms of biocompatibility structural
stability and a good tear resistance for sewing. The
sponges could support the proliferation of human
keratinocytes (HaCat) and gingival fibroblasts (GF)
cells (Chiaoprakobkij et al. 2011). A total of 30
6-month-old New Zealand white male rabbits have
been tested for laryngeal reconstruction, which is
made of bacterial cellulose. Results demonstrated that
the material caused no significant foreign-body reac-
tion and remained stable throughout 4 months of
follow-up (de Souza et al. 2011).
What should be mostly concerned in this field
BC as a commercially available material for biomed-
ical applications has attracted great interest for various
benefits over its synthetic polymer counterparts.
However, the relatively poor biodegradability in the
human body for the lacking of appropriate glycoside
hydrolases, perhaps was regarded as the obstacles in
hindering further application of this material. Besides,
the biodegradable materials must possess a controlla-
ble biodegradation rate that could match with the tissue
regeneration rate to allow the cells to grow before
bioabsorption of the scaffold during the healing
progress (Wang et al. 2011b). In order to solve this
problem, Peng et al. (2012) prepared a new kind of
degradable oxidized bacterial cellulose (OBC) by
oxidizing BC in the presence of nitrogen dioxide
(NO2). Hu and Catchmark (2011) developed a bioab-
sorbable bacterial cellulose (BBC) material, which
integrated one or more cellulose degrading enzymes
(cellulases). Both of their degradation rate could be
adjusted under the controllable preparation progress.
From another point of view, BC degraded in vivo
would probably make nanofibers release from the
implanted tissue. Hence, it is necessary to concern
about the safety and toxicology of BC especially for a
longer period of time (up to 1 year) (Pertile et al. 2012).
Besides plenties of researches concentrating on this
field, some companies have launched several com-
mercial products especially in wound healing system.
A Brazilian company, BioFill Produtos Bioetecnolog-
icos (Curitiba, PR Brazil) developed a series of
products based on BC, including the following:
Biofill� and Bioprocess� (used in the therapy of
burns, ulcers as temporary artificial skin), and Gengi-
flex� (applied in treatment of periodontal diseases)
(Jonas and Farah 1998). Another company, Xylos
Corporation in the US, has developed several medical
devices using BC since 1996. From then on, the
company kept improving its own technology and
successfully obtained the Food and Drug Administra-
tion (FDA) approval on its products. The XCell�
family offered by the company has been marketed in
the US since 2003 (Czaja et al. 2006). Unlike BC
dressings manufactured by Biofill�, the Xcell� prod-
uct is claimed to have a dual-function of both
hydration and absorption to maintain the ideal mois-
ture balance, which is originally considered to be a
contradiction and hardly obtained in practice. It is
based on the fact that it conforms to wounded and
intact skin differently (Alvarez et al. 2004). Besides
the problems mentioned, a particularly efficient strain
without frequent mutations over time and large-scale
fermentation system with high performance should be
further investigated for a breakthrough to improve the
commercial application in medical field.
BC used for sewage purification
Discarding liquid effluents containing heavy metals,
or organic dyes without treatment is of great concern.
Due to their toxic effect to the health of human beings
and other livings, it is important to remove the
pollutants from wastewater before it is drained.
Functionalized BC used for adsorption
BC is attractive to be prepared as an adsorbing
material for the remedy of pollution problems due to
its advantageous properties: (1) high mechanical
strength and good chemical stability, which are
usually lacked in natural sorbents such as chitosan
(Mladenova et al. 2011), and (2) ultrafine nanofiber
network and high specific surface area, which is
closely related to adsorption efficiency. Oshima et al.
Cellulose (2014) 21:1–30 13
123
(2008) prepared phosphorylated bacterial cellulose
(PBC) as an ion-exchanger that exhibited a high
adsorption capacity for various transition metal ions
and lanthanide ions. As large adsorbates cannot access
internal adsorption sites, adsorption of large adsor-
bates proceeds only at the surface of the adsorbent.
Oshima et al. (2011) found PBC showed much higher
adsorption capacity for macromolecules such as
proteins than that of phosphorylated plant cellulose
(PPC) under identical conditions due to its larger
surface area (Fig. 12).
To increase the metal ion adsorption of BC, it was
chemically modified by introducing different com-
plexing groups. Recently, various chemically
modified BCs as new adsorbents or catalyst for
pollutants in wastewater have been developed. Dieth-
ylenetriamine BC (EABC) (Shen et al. 2009), carbo-
xymethylated BC (CM-BC) (Chen et al. 2009b) and
amidoximated BC (AM-BC) (Chen et al. 2009a,
2010b) have been prepared for adsorptive removal of
Cu2? and Pb2?, and their adsorption properties as well
as the adsorption kinetics and adsorption isotherms
were studied. The authors suggested that the mecha-
nism for the adsorption of Cu2? onto AM-BC could be
mainly attributed to the formation of metal complexes
with both the nitrogen atoms in the amidoxime groups
and the oxygen atoms in the hydroxyl groups. While in
the adsorption process for Pb2?, precipitation played
Fig. 12 Conceptual
illustration of adsorption of
large biomacromolecules
such as proteins as well as
small molecules on PBC and
PPC. (Reprinted from
Oshima et al. 2011 with
permission from Elsevier)
14 Cellulose (2014) 21:1–30
123
an important role along with electrostatic interactions,
although chelation action also worked during the
adsorption process. Yin et al. (2011b) modified BC
with succinic anhydride in different methods, and its
adsorption capacity as well as mechanism of Cu2? was
investigated, the results showed that the adsorption
was affected by the morphology and the degree of
substitution (DS) of adsorbents.
Since BC nanofibrils networks have been used as a
template for the non-aggregated growth of magnetic
particles (Olsson et al. 2010b), some magnetite
nanoparticles (MNPs) such as hematite, magnetite,
and goethite (Gimenez et al. 2007), which have been
used as effective adsorbents for metal removal were
also introduced to BC to enhance the metal removal
performance. Nata et al. (2011) prepared aminated
magnetite-BC nanocomposite via one-pot thermal
synthesis in solution phase. The magnetite nanoparti-
cles deposited along the BC nanofibrils played a
synergistic effect on arsenic adsorption with surface
functionalized amine groups. In addition, the com-
posite containing magnetic particles possess super-
paramagnetism, so it can be recollected under a
magnetic field. Timko et al. (2004), Zhu et al. (2011)
prepared spherical Fe3O4/BC nanocomposites used for
removing heavy metal ions from sewage. In their
work, the spherical Fe3O4/BC nanocomposites can be
reused again after the adsorbed heavy metal ions are
eluted. In Nata’s work (Nata and Lee 2010), an easily
retrievable carbonaceous pellicle was synthesized by
one-step mild hydrothermal process to solve the
difficulties in recovery which usually encounters in
the direct application of carbonaceous nanoparticles
for heavy metal ion adsorption. Moreover, acrylic acid
was employed during hydrothermal carbonization to
increase the surface carboxyl content and enhance its
metal ion adsorption capacity, with the result of a high
adsorption capacity towards Pb2? and Fe3?, approx-
imately, 200 and 1,134 mg/g, respectively.
BC used as a matrix in catalyzing
Apart from its applications in absorption of metal ions
from wastewater, BC was provided as a template for
the synthesis of various inorganic nanomaterials, such
as CdS (Yang et al. 2011a), TiO2 (Sun et al. 2010c;
Zhang et al. 2011c), Pa0 (Vyjayanthi and Suresh
2010), ZnO (Hu et al. 2010), Cu2O (Liu et al. 2011)
nanoparticles for efficient catalysts for pollutant
abatement.
Sun et al. (2010b) prepared a novel Pd–Cu/BC
composite catalyst used for water denitrification. In
this research, BC was used as a supporting material,
and Pd–Cu nanoparticles of about 4.0 nm were
homogeneously and densely precipitated on BC
surface for its nanofibrillar structure and large specific
surface area. The Pd–Cu/BC catalyst exhibits high
selectivity to the formation of nitrogen up to 94.4 %
and a relative high catalytic activity which is twofold
compared to Mikami’s report (Mikami et al. 2003).
The deposited inorganic nanoparticles were well-
dispersed on BC surface showing high reactivity as a
catalyst for water-soluble textile dyes.
Comparing to commercial photocatalyst P25, Sun
Dongping’ group prepared much better photocatalytic
organic–inorganic hybrids with BC substrate and
nanoparticles such as TiO2 (Sun et al. 2010c) and
CdS (Yang et al. 2011a). The nitrogen-doped BC/TiO2
hybrid nanofibers prepared by a controlled surface
hydrolysis method exhibited an increase in surface
area of much as 156- and a 25-fold increase of pore
volume compared with the BC fibers (Fig. 13). The
photocatalytic activity of BC/TiO2 hybrid nanofibers
with larger surface-to-volume ratio and smaller crys-
tallite size is much higher than that of P25 when
degraded methyl orange (MO) under UV irradiation.
Similarly, when homogeneously incorporated with
CdS nanoparticles the hybrid nanofibers showed high-
efficiency photocatalysis capacity by which 82 %
methyl orange (MO) was degraded under visible light
irradiation for 90 min. The degradation rates for
5-cycle reuses were 82, 80.4, 78.6, 78, and 77.3 %,
respectively. The slightly decreased photocatalytic
reactivity (Fig. 14) of the photocatalyst indicates a
relatively superior stability and reusability in practical
water treatment.
Applications in electrical, magnetic and optical
fields
As a natural polymer, BC has obtained considerable
attention on account of its high tensile strength and
crystallinity, nanoscale and biocompatibility. Many
new application fields were found nowadays, such as
electrical materials, optical materials, magnetic
Cellulose (2014) 21:1–30 15
123
materials. Therefore, functionality nanomaterials have
been attracted great scientific interest along with the
increasing demand of new technologies for the
development of electronic devices, sensors, intelligent
clothes, to be employed in several fields including
biology, medicine, defense, agriculture, etc.
Electrical materials
Due to their high strength and stiffness associated with
renewability, biocompatibility and biodegradability,
cellulose nanofibers act as very promising support
materials for conductive additives (Iguchi et al. 2000).
We know that BC is a non-conducting material, but
it turns into conduct when some conductive nanom-
aterials are added in. Muller et al. (2011, 2012) coated
BC surface with both conductive polypyrrole (PPy)
and polyaniline (PANI) through in situ oxidative
chemical polymerization by using FeCl3�6H2O as
oxidant. As a result, a continuous conducting layers
were formed on the surface of BC nanofiber with the
constitution of a core–shell structure. It is reported that
the electrical conductivity of the composites are
dependent on oxidant and monomer concentration as
well as the reaction time.
Fig. 13 SEM and TEM images of BC nanofibers. a A general view of the nanofibers. b A TEM image of the nanofibers. c–d TEM
images of BC/TiO2 hybrid nanofibers (Reprinted from Sun et al. 2010C with permission from Royal Society of Chemistry)
Fig. 14 The decrease of MO concentration with visible light
irradiation by recycling use of CdS/BC. C is the dye concentra-
tion and C0 is the initial concentration of MO (Reprinted from
Yang et al. 2011a with permission from Elsevier)
16 Cellulose (2014) 21:1–30
123
Similarly, an ordered flake-type morphology of BC/
PANI nanocomposites were prepared with an out-
standing electrical conductivity and high special
capacitance (Wang et al. 2012). The conductivity of
BC/PANI nanocomposite films obtained could be as
high as 5.1 S/cm, which is more than 100 times
improvement compared with the values from the latest
literature (Chan et al. 1995, 2010a; Lee et al. 2012),
while the mass-specific capacitance could reach a
level of 273 F/g at a current density 0.2 A/g, which is
comparable to that of composites composed of 20 wt%
of multiwalled carbon nanotubes and 80 wt% of PANI
(305 F/g) (Khomenko et al. 2005) and that of
graphene-PANI nanocomposites (*300 F/g) (Gomez
et al. 2011). Both of the superior characteristics could
be attributed to the well-controlled composite mor-
phologies with good dispersion and suitable size of
PANI flakes (Fig. 15). It is estimated that DMF plays
an important role in abundant aniline dispersion and
self-assembly onto BC nanofibers and in its 3D
networks for polymerization. Furthermore, the com-
posites also behave a superior electrochemical stabil-
ity with about 94.3 % of initial capacitance after 1,000
cycles. It could be ascribed to the strong interaction
between the BC core and the PANI shell.
Besides, some of BC derivatives have also been
found to be conducting. Wang et al. (2008) reported
the preparation of benzoylated bacterial cellulose
(BBC) through esterification of BC with benzoyl
chloride. Benzoyl chloride reacts with the hydroxyl
groups on the glucopyranose unit of BC, and eventu-
ally benzoyl substituents are attached to the BC
backbone to form the BBC, which is one of the
potential candidates for sensors, high-level piezoelec-
tric and optical materials. With gradual substitution,
the molecular chain of the BBC becomes semirigid
and displays an interesting thermotropic liquid crys-
talline phase.
BC membranes were also used as flexible substrates
for the fabrication of Organic Light Emitting Diodes
(OLED) (Legnani et al. 2008), which holds great
promise in research dedicated to the development of
new optoelectronic and photonic devices. These
electroluminescent (EL) devices have the advantages
of being easy to make, with low operating voltages,
and the possibility of a wide selection of emission
colors through the molecular design of organic
materials. Carbon paste electrode (CPE) consisting
of carbon powder and water-immiscible liquid binder
is one of the most commonly used electrodes in
electrochemical investigations. A novel nano-dimen-
sion carbonized BC based on CPE (BCPE) was
developed for the purpose of enhancing the sensitivity
and selectivity according to the report of Liang et al.
(2009).
Liang et al. (2012) have developed a simple and
inexpensive method to fabricate highly conductive
and stretchable composites using BC pellicles as
starting materials. The prepared pyrolyzed BC (p-BC)/
polydimethylsiloxane (PDMS) composites exhibit a
high electrical conductivity of 0.20–0.41 S/cm, which
is much higher than conventional carbon nanotubes
and graphene-based composites. It is believed that the
outstanding electromechanical properties of the com-
posites are due to the robust and preformed 3D
networks of the p-BC aerogels that provide intercon-
nected pathways through which electrons can quickly
move.
Magnetic materials
Magnetic nanomaterials have been investigated for
biomedical, data storage and device applications.
Materials combining BC with magnetic nanoparticles
are interested for the current investigation. In previous
methods, nanoparticles were mixed directly with
polymer matrix, but nowadays, lots of new approaches
are appearing.
Fig. 15 FE-SEM images of BC/PANI nanocomposites with
86 wt % PANI prepared from DMF/H2O (1:2, v/v) at 0 �C
(Reprinted from Wang et al. 2012 with permission from
American Chemical Society)
Cellulose (2014) 21:1–30 17
123
The fibrous network structure, apart from providing
high mechanical strength, offers micro/nanoporous
spaces, which can be used as reaction chambers for
precipitation of nanoparticles with the BC fibers
providing a support structure to hold the particles.
Vitta et al. (2010) used BC as a support material to
precipitate Ni nanoparticles at room temperature by
chemical reduction of Ni-chloride hexahydrate. The
Ni loaded onto bacterial cellulose is found to be
ferromagnetic at room temperature.
Polymer-nanoparticle composites which combine
the properties of the polymer and the nanoparticle in a
synergistic manner have attracted great attention for
the use in various fields. Zhang et al. (2011a) prepared
a flexible magnetic membrane based on BC with
amphiphobicity. It was prepared firstly by the in situ
synthesis of the Fe3O4 nanoparticles on the BC
nanofibers and then the fluoroalkyl silane (FAS)
modification. The fabrication procedure and sche-
matic diagram of testing is shown in Fig. 16. The
hierarchical micronanostructure of micro- and nano-
sized Fe3O4 deposited on the fibers with the diameter
of 80–100 nm in 10 mol/L FeCl2�4H2O/20 mol/L
FeCl3�6H2O appropriately increases its surface rough-
ness, which leads to its highest amphiphobicity. The
fluorinated membrane with appropriate roughness
showed the highest water contact angle (WCA) of
130 �C and oil contact angle (OCA) of 112 �C. Proper
roughness can enhance hydrophobicity of a solid
surface leading to high contact WCA (Marins et al.
2011). This study indicated an effective way to
fabricate the flexible and magnetic BC membranes
with self-cleaning properties by increasing the surface
roughness and decreasing the surface energy of
material.
Optical materials
A substantial amount of work has been carried out in
the area of nanocomposite materials for optical
Fig. 16 Schematic illustration for the flexible magnetic nanohybrid membrane with amphiphobic surface (Reprinted from Zhang et al.
2011a with permission from Elsevier)
18 Cellulose (2014) 21:1–30
123
applications. Among them, cellulose-based nanocom-
posite is one of the most potential candidates. It has the
properties of light transmittance for its nano-sized
fibers, which are smaller than the wavelength of
visible rays. Cai and Yang 2011 prepared a biode-
gradable, biocompatible and optically active poly(3-
hydroxybutyrate)/bacterial cellulose PHB/BC nano-
composite and measured its light transmittance to
investigate how the BC affects the transparency of the
nanocomposite. The result showed that the transpar-
ency of the PHB/BC nanocomposite was high due to
the homogeneous nano-sized spherulite and nanofibril
of PHB and BC. Lots of researchers have used
cellulose nanofibril to prepare optically transparent
composites which have potential applications such as
display devices, coatings and lenses.
BC hydrated membranes present nanometric retic-
ulated structure (Fig. 2) that can be used as a template
in the preparation of new organic–inorganic hybrids.
BC-silica hybrids (Fig. 17) were prepared from BC
membranes and tetraethoxysilane (TEOS) at neutral
pH conditions at room temperature (Barud et al. 2008).
The new hybrids are still stable even up to 300 �C and
display a broad emission band under UV excitation. It
can be assigned to electron–hole recombination in
oxygen related defects located on the particles surface.
The tunable emission color is an interesting property
observed for these new hybrids with new perspectives
of applications in optical devices. This research opens
a new direction in search for new phosphors.
The photochromic BC nanofibrous membranes
containing 10,30,30-trimethyl-6-nitrospiro(2H-1-benz-
opyran-2,20-indoline) (NO2SP) were successfully
prepared by surface modification of BC nanofibers
with spiropyran photochromes by Hu et al. (2011d).
The result indicates that the surface modification with
spiropyran photochromes expands new applications of
BC nanofibers and those photochromic nanofibers
with excellent photosensitivity (Fig. 18) have great
potentials for sensitive displays, biosensors and other
optical devices.
Bacterial cellulose nanowhiskers
Nanowhisker is usually regarded as a category of
organic filler, which could act as the reinforcing
elements with the morphology of the whisker-like
nanofibrils. Each cellulose nanofiber can be consid-
ered as a string of cellulose crystals which are linked
by disordered or paracrystalline regions. With the
purpose of extracting nanowhiskers from its precursor,
cellulosic materials are usually subjected to hydrolysis
in order to removing the amorphous domains and
retaining highly crystalline residue. Afterwards, nano-
whiskers could be obtained in a stable suspension,
followed by repeated steps of centrifugation and
rinsing. Due to its high stiffness and relatively ease
of preparation, cellulose nanowhiskers have received a
great deal of interest as a reinforcing agent in
nanocomposites, especially when their comparatively
lower density is taken into account (i.e. possessing
~3.5-fold of specific modulus compared to steel)
(Soykeabkaew et al. 2012). It could be predicted that
natural fibers are a viable alternative to inorganic/
mineral based reinforcing fibers in commodity ther-
moplastic composite materials as long as the right
processing conditions are used and for applications
Fig. 17 SEM images of BC membranes (left) and BC-silica (66 wt %) composite (right) (Reprinted from Barud et al. 2008 with
permission from Springer)
Cellulose (2014) 21:1–30 19
123
where higher water absorption may be not so critical
(Azizi Samir et al. 2005).
As to bacterial cellulose, it is well known for its
superior properties over plant cellulose. Bacterial
cellulose having high purity, high crystallinity and
excellent biological affinity, is the ideal reinforcing
component for biopolymer composites (Tashiro and
Kobayashi 1991). It has a high Young’s modulus up to
114 GPa (Habibi et al. 2010). In the case of BC, there
is no hemicellulose or lignin to remove. As a result, the
extraction method pointed that BC nanofibers are
obtained in the centrifugation precipitate instead of the
supernatant which is usually preserved in the plant
cellulose hydrolysis because impurities usually remain
in the solid precipitate (Martınez-Sanz et al. 2011a)
and, thus, the yield can be enhanced to the level of
89 % based on the dry weight of bacterial cellulose
(Martınez-Sanz et al. 2011b; Olsson et al. 2010a)
versus yields around 1–5 % when the whiskers are
obtained from the liquid supernatant. Besides, a higher
aspect ratio (L/d, L being the length and d the
diameter) of the nanofiber is also a contributor in
increasing the stress transfer efficiency. An increased
aspect ratio will increase the surface area of the
reinforcing phase that is effectively in contact with the
polymer and facilitates easy stress transfer through
filler polymer matrix adhesion (George 2012).
Methods for acid hydrolysis
The most commonly employed method for the
processing of cellulose nanocrystals is by employing
acid hydrolysis. The acid treatment leads to the
removal of the amorphous domains that are regularly
distributed along the microfibers, and leads to the
formation of rod-like cellulose nanocrystals (Fig. 19)
(Habibi et al. 2010).
Martınez-Sanz et al. (2011a, b, 2012) achieved the
BC nanowhiskers by the method of sulfuric acid
hydrolysis. Sulfuric acid hydrolysis leads to stable
aqueous suspensions of cellulose nanocrystals which
are negatively charged and thus, do not tend to
aggregate. A dispersion of individual whiskers can be
demonstrated by the phenomenon of flow birefrin-
gence (Azizi Samir et al. 2004). The BC nanocrystals
(BCNC) which were well separated in solution would
show flow birefringence, as shown in Fig. 20 (Yun
et al. 2010).
During the hydrolysis process, esterification of the
surface hydroxyl groups from cellulose takes place
and as a consequence, sulfate groups are introduced
(Ranby 1949). Unfortunately, as is shown in Fig. 21
(Martınez-Sanz et al. 2011a), even treated for a short
period, the sulfate groups caused a significant decrease
in degradation temperatures and an increase in char
fraction confirming that the sulfate groups act as flame
retardants. However, with the typical processing
temperatures for thermoplastics often exceeding
200 �C, the thermostability of the crystals is important
for this application (Roman and Winter 2004).
The Spanish group optimized the process by
changing the concentration of sulfuric acid and the
time for hydrolysis. The effect of neutralization and
dialysis after the acid treatment on the thermal
stability was also studied. They concluded that
neutralization produced a slight increase in the
crystallinity index, and, most importantly, it led to a
remarkable increase on the BC nanofibers thermal
stability, which is even higher than the native BC,
while the dialysis applied made no sense. As they
explained that, the crystalline domains which are
thermally stronger than the amorphous fractions, and
sulfate groups introduced during hydrolysis are further
removed (Martınez-Sanz et al. 2011a).
Fig. 18 The fluorescent effect of BC-NO2SP membranes (0.06
wt % NO2SP) under different UV irradiation time of 365 nm
UV light conditions: a before UV irradiation, b after UV 10 s,
c after UV 30 s, d after UV 60 s, and e after UV 120 s
(Reprinted from Hu et al. 2011d with permission from Springer)
20 Cellulose (2014) 21:1–30
123
An alternative is to use hydrochloric acid, which
produces nanocrystals without any surface charges
unlike sulfuric acid hydrolysis produces. However,
the absence of such surface charges promotes the
aggregation of cellulose through hydrogen bonding
(George 2012). Additionally, new microporosity is
observed in HCl treated cellulose, especially in the
upper fraction which refers to the smaller suspended
nanofibers. It is hypothesized that this new micropo-
rosity results either from the delamination of the
cellulose crystal sheets when the amorphous cellu-
lose is removed; or from the hydrolysis of amorphous
cellulose in between bundles of elementary fibrils
(Guo and Catchmark 2012).
Methods for cellulases hydrolysis
Preparation of nanofibers by concentrated acid solu-
tion is energy consuming, environmentally hazardous,
poor thermal stability and also significantly lower
degree of polymerization (DP), which therefore
reduced its mechanical property in nanocomposites
(Zimmermann et al. 2004). Thus a novel method to
produce cellulose nanocrystals which retains some of
the native structural properties of BC was tested using
a commercially available cellulase preparation. The
widely-accepted mechanism for enzymatic cellulose
hydrolysis suggests that three different types of
cellulases work synergistically in a cellulase complex
Fig. 19 Transmission electron micrograph from a dilute suspension of hydrolyzed BC
Fig. 20 Photograph of the dispersions of BCNC in water after
hydrolysis in H2SO4 solution for 1 h (a), 2 h (b) and 3 h (c),
viewed through crossed polarizers (Reprinted from Yun et al.
2010 with permission from Taylor and Francis)
Fig. 21 DTG curves of native BC, BCNW treated with H2SO4
for 2 and 48 h (Reprinted from Martınez-Sanz et al. 2011a with
permission from Elsevier)
Cellulose (2014) 21:1–30 21
123
during this process (Lynd et al. 2002; Gusakov et al.
2007). George et al. (2011) utilized the cellulase at its
optimum conditions in the process of hydrolysis, and
the results depicted in Fig. 22 revealed a better
thermal and strength properties compared to the
nanocrystals obtained from sulfuric acid hydrolysis.
As what we were expected that, when incorporated
the nanofibers into polyvinylalcohol (PVA), the
nanocomposites exhibited higher melting temperature
(Tm) and enthalpy of melting (DHm) than those of
pure PVA, suggesting that the addition of nanocrystals
modified the thermal properties of PVA.
When BCNC acts as a filler in composite, it usually
improves the reinforcement notability resulting from
the load bearing can be shared with or concentrated
into the nanofiber. The modified mechanical proper-
ties combined with nanocrystal are listed in Table 2 by
George group (2012, 2011), and the BCNC in the
nanocomposites is extracted from cellulase and
hydrochloric acid respectively.
Data from table listed above reveals that BCNC
produced by relatively mild enzyme treatment makes
its composite exhibit higher tensile strength/modulus
(*twofold to matrix itself when 4.0 wt% content)
compared with the one suffered hazardous acid
hydrolysis. It probably due to the relatively higher
DP and crystallinity are preserved when treating with
specific cellulase. Data from the column of elongation
at break implies that PVA behaves more flexible than
gelatin and the addition of BCNC could make both of
the matrices more stiffness.
Novel applications of BCNC
In addition to its excellent mechanical properties, BCNC
which spread over the surface of glass beads (diameter
3 mm) could also be able to efficiently stabilize at the oil/
water interface when its surface charge density has been
modulated by various postsulfation/desulfation treat-
ments. SEM images of Fig. 23 revealed the surface
organization in detail. The colloidal-size particles
anchored at the oil–water interface formed the so-called
Pickering emulsions which not only present good
mechanical properties, but much fewer particles are
required to produce good stability, thereby leading to a
reduction in the use of hazardous surfactants (Binks 2002;
Aveyard et al. 2003). Kalashnikova et al. (2012) deduced
that the amphiphilic character reside in the crystallin
organization at the elementary brick level, which the
(200)b/(220)a hydrophobic edge plane appears respon-
sible for the wettability of the cellulose nanocrystals at the
oil/water interface, and therefore, its accessibility will
determine the ability to produce stable emulsions.
One of the most interesting characteristic of
cellulose nanofibers aqueous suspensions is their
ability of self-organization into stable chiral nematic
phases. Hirai et al. (2009) demonstrated that BCNC
suspensions at concentrations above 0.42 wt%
Fig. 22 TGA and DTG curves of a bacterial cellulose
nanocrystals obtained by sulfuric acid hydrolysis and b bacterial
cellulose nanocrystals obtained by enzyme hydrolysis (Rep-
rinted from George et al. 2011 with permission from Elsevier)
Table 2 Mechanical properties of BCNC/PVA and BCNC/
gelatin nanocomposites. (Reprinted from George et al. 2011
and 2012 with permission from Elsevier)
BCNC content in
composites
(wt %)
Tensile
strength
(MPa)c
Tensile
modulus
(GPa)c
Elongation
at break
(%)c
0a 62.5 ± 4.5 1.8 ± 0.3 154.9 ± 20
1a 94.7 ± 5.2 2.3 ± 0.2 148.7 ± 18
2a 106.2 ± 4.1 2.8 ± 0.1 142.0 ± 22
3a 117.2 ± 6.8 3.1 ± 0.2 138.8 ± 19
4a 128.5 ± 5.8 3.4 ± 0.1 132.1 ± 21
0b 83.7 ± 3.2 2.19 ± 0.05 33.7 ± 1.6
1b 88.7 ± 4.8 2.23 ± 0.06 33.1 ± 1.8
2b 95.1 ± 3.9 2.27 ± 0.07 29.8 ± 2.2
3b 103.1 ± 4.7 2.34 ± 0.06 27.5 ± 1.9
4b 108.6 ± 5.1 2.35 ± 0.07 23.4 ± 1.8
a The content of BCNC extracted from cellulase in PVA
matrixb The content of BCNC extracted from hydrochloric acid in
gelatin matrixc Mean ± SE (n = 10)
22 Cellulose (2014) 21:1–30
123
separated into the isotropic and chiral nematic phases
with a clear phase boundary (Fig. 24).
However, cotton cellulose nanocrystals (CCNC)
extracted from Whatman No. 1 filter paper powder
(98 % cotton fiber) form an anisotropic phase above a
critical concentration of around 4.5 wt% (Dong et al.
1998), and 5.3 wt% for wood (black spruce pulp)
cellulose (Beck-Candanedo et al. 2005). They also
revealed that the aspect ratio of cotton nanocrystals is
24, and that of wood nanocrystals is 29, while the data
is 44 and 73 regarding to the upper and lower layers of
the separated phase of BCNC solution respectively.
Besides, the surface charge density (ca. 0.05e nm2) of
BCNC, however, is approximately one-seventh that of
the corresponding value for wood cellulose. It is
proposed that the much lower critical concentration
for the BCNC suspension could be probably attributed
to a larger aspect ratio, a lower level of surface charge
density and the rectangular shape of the cross section
that pertained only in BC fibers.
Using this process to orient cellulose microcrystals,
Revol et al. (1997, 1998) created an important new
material with original optical properties. The wave-
length of reflected light can be controlled by adjusting
the ionic strength of the suspension. These new
materials have a high application potential like those
for security papers (Azizi Samir et al. 2005).
Other applications
Due to its excellent properties, BC has attracted much
attention as a new functional material applied in paper
production (Mormino and Bungay 2003). In general,
the presence of bacterial cellulose in papermaking
semi-products can lead to the improvement of their
strength properties (Surma-Slusarska et al. 2008b).
Surma-Slusarska et al. (2008a) studied the strength
properties of three different papermaking semi-pro-
ducts (i.e. unbeaten, bleached birch and pine sulphate
pulps) with bacterial cellulose. The breaking length
and tear index were improved by joining bacterial
cellulose with pulp fibers. In addition to its function as
a fillers aid, BC also can be used for the preparation of
Fig. 23 SEM images of polymerized styrene/water emulsions stabilized by a bacterial cellulose nanocrystals (BCN) and b cotton
cellulose nanocrystals (CCN) (Reprinted from Kalashnikova et al. 2012 with permission from American Chemical Society)
Fig. 24 Phase behavior of
BC nanocrystals dispersed
in deionized water as a
function of the total
concentration after 25 days
of standing (Reprinted from
Hirai et al. 2009 with
permission from American
Chemical Society)
Cellulose (2014) 21:1–30 23
123
specialized paper once modified. Basta and El-Saied
(2009) introduced phosphorous element in the BC
chain to prepare a flame-retardant paper by substitut-
ing glucose in cultivation medium with glucose
phosphate. The added phosphorylated bacterial cellu-
lose (PBC) not only enhanced the strength and
durability of pulp greatly when integrated into paper
but also controlled smoke generation and toxicity
when burning by minimizing the formation of levo-
glucosan by lowering the decomposition temperature
of cellulose. As a result, incorporating 5 % of the PBC
with wood pulp during paper sheet formation was
found to significantly improve fire resistance proper-
ties compared to paper sheets with native BC.
Wang’s group fabricated two novel sensors (a
humidity sensor (Hu et al. 2011c) and a formaldehyde
sensor (Hu et al. 2011a)) by coating quartz crystal
microbalance with BC membrane and polyethylene-
imine/BC membranes, respectively. Both of the two
sensors showed high sensitivity with good linearity
and exhibited a good reversibility, indicating that BC
membrane materials could act as a promising candi-
date for mass production of the high performance low-
cost sensors. And another application for BC was
proposed by Hu’s group (Hu et al. 2011d), who
selected BC to restore the vulnerable historic silk
fabrics due to its good mechanical property and
degradability, instead of the traditionally used syn-
thetic polymers. Because synthetic polymers have the
problems that they are difficult to be removed without
damaging to the historic silk textiles, for most of the
synthetic polymers can only be dissolved in either
organic solvent or degraded at extreme conditions.
Due to its primary structure which is similar to plant
cellulose, together with its ultrafine and highly pure
fiber network structure, BC shows potential applica-
tions in explosive industry as substituent of plant
cellulose according to Sun et al. (2010a), who first
prepared bacterial cellulose nitrate (NBC) from BC. It
is not so difficult to control in the nitration process
because of the relatively high chemical purity and is
expected to perform as an advanced energetic mate-
rial. In addition, the proton exchange membrane fuel
cells in which BC is used as membrane electrode
incorporated with platinum (Pt) nanoparticles was
firstly fabricated by Sun and his coworkers (Yang et al.
2009). With the distinctive interconnecting porous
structure, BC owns the ability to incorporate fine
divided Pt nanoparticles with mean diameter of
3–4 nm well impregnated into the BC fibrils. The
maximum output of the fuel cell on the basis of Pt/BC
is 12.1 mW/cm2 which is comparable to the value of
Pt/C electrolyte of 19.9 mW/cm2.
Conclusion
Generally speaking, bacterial cellulose has attracted
considerable interests in various application fields no
matter acting as a matrix or using in its modified state.
Compared to other synthetic or natural macromole-
cule, BC is distinctive in several aspects such as
unique nanostructure, high purity, high crystallinity,
large water holding capacity, higher Young’s modu-
lus, excellent biodegradability and biological affinity
etc. However, despite of all these advantages, the
relative high cost, and poor durability especially in
moist environment, could be a hindrance to its wide
application. So the research around fermentation for
enhancing productivity should be concentrated on
further. And BC probably prefers to using in its dried
state or being enclosed by other substance, except for
the disposable applications such as facial mask and
medical wound healing etc.
Acknowledgments We acknowledge the financial support
from State 863 Projects (2011AA050701), the Fundamental
Research Funds for the Central Universities (No.
30920130121001), and a Project Funded by the Priority
Academic Program Development of Jiangsu Higher Education
Institutions (PAPD, China).
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