ler, bom

Carbohydrate Polymers 313 (2023) 120850
Contents lists available at ScienceDirect
Carbohydrate Polymers
journal homepage: www.elsevier.com/locate/carbpol
Review
Conductive bacterial cellulose: From drug delivery to flexible electronics

Artur Prilepskii *, Vitaly Nikolaev, Anastasiia Klaving
ITMO University, Laboratory for Bioactive Materials in Tissue Engineering, 9, Lomonosova str., Saint Petersburg 191002, Russian Federation
A R T I C L E I N F O A B S T R A C T
Keywords: Bacterial cellulose (BC) is a chemically pure, non-toxic, and non-pyrogenic natural polymer with high me
Bacterial cellulose chanical strength and a complex fibrillar porous structure. Due to these unique biological and physical prop
Conductivity erties, BC has been amply used in the food industry and, to a somewhat lesser extent, in medicine and
Flexible electronics
cosmetology. To expand its application the BC structure can be modified. This review presented some recent
Conductive polymers
developments in electrically conductive BC-based composites. The as-synthesized BC is an excellent dielectric.
Conductive polymers, graphene oxide, nanoparticles and other materials are used to provide it with conductive
properties. Conductive bacterial cellulose (CBC) is currently investigated in numerous areas including electrically
conductive scaffolds for tissue regeneration, implantable and wearable biointerfaces, flexible batteries, sensors,
EMI shielding composites. However, there are several issues to be addressed before CBC composites can enter the
market, namely, composite mechanical strength reduction, porosity decrease, change in chemical characteristics.
Some of them can be addressed both at the stage of synthesis, biologically, or by adding (nano)materials with the
required properties to the BC structure. We propose several solutions to meet the challenges and suggest some
promising BC applications.
1. Introduction by external stimuli. Such devices have to be based on a certain material,

the parameters of which would be similar to those of the body tissue, and
Conductive materials are required in many areas. These materials which would be easy to fabricate. So far, scientists have relied on chi
can include biointerfaces for communication between electronic devices tosan, alginate, BC and other natural polymers. Among the latter, BC
and the human body (Cai et al., 2017) or artificial tissues, for example, presents a unique 3D fibrillar network capable of organizing multilayers
heart tissue that are used in regenerative medicine (G. Jin & Li, 2015). with high porosity and large surface area, which opens up unrivalled
They are essential because simple implantation of electronics into the opportunities for biomedical application (Stanescu et al., 2021). BC
human body is cyberpunk fiction. This is primarily due to immune properties have been widely studied (Blanco Parte et al., 2020). It is
response and eventual infections, the impossibility to mimic the me highly biocompatible, biodegradable, and possesses promising charac
chanical parameters of tissues and create flexible and durable interfaces teristics of strength and a particular fibrillar internal structure (Iguchi
(Bullard et al., 2020; Cantillon et al., 2018). Today, scientists and en et al., 2000). Some materials based on BC are already available on the
gineers have succeeded in producing implantable pacemakers. Howev market (Mbituyimana et al., 2021). These include vascular implants
er, even this advanced technology presents multiple challenges (Gillam (Schumann et al., 2009), wound dressings (Sulaeva et al., 2020), and
et al., 2018). On the other hand, with life expectancy increasing, more cosmetics (Bianchet et al., 2020).
implanted or modified parts of the human body are required (Meng & However, to be used as a basis for electronic devices or conductive
Sheybani, 2014). tissues BC has to be modified. Unmodified BC is a dielectric with con
The main categories of “devices” necessary to address this issue are ductivity in the range of 10-6–10-8 S/cm (Erbas Kiziltas et al., 2016) or
electrodes, biointerfaces, sensors, power supplies, artificial tissues, and even 10-13 S/cm (Müller et al., 2012) and resistance of approximately
drug delivery vehicles. They can either work separately or can be 108 Ω ⋅ cm (Lin et al., 2013). This makes it an excellent insulator, which,
combined into a single complex device. The essential challenges that by the way, can also be adequately used for designing electronic im
need to be addressed are the control of their mechanical, chemical, and plants (Zhuravleva et al., 2018). It is carbonizing BC and introducing
conductive properties, biocompatibility, and the ability to control them various conductive dopants into its structure that can significantly
* Corresponding author.
E-mail address: [email protected] (A. Prilepskii).
https://doi.org/10.1016/j.carbpol.2023.120850
Received 14 December 2022; Received in revised form 22 March 2023; Accepted 23 March 2023
Available online 29 March 2023
0144-8617/© 2023 Elsevier Ltd. All rights reserved.
A. Prilepskii et al. Carbohydrate Polymers 313 (2023) 120850
increase its conductivity (L. Liang et al., 2020). However, this leads to a maximum of its biomechanical properties. If in some cases the original
degradation in its mechanical properties and biocompatibility. Some BC has been subjected to homogenization to obtain a composite, this will
approaches to this issue involve complete disintegration of BC structure be specially indicated.
using various homogenizers (X. Xu et al., 2021). This results in forming For acronyms of BC composites, we use our own designations for
various shapes from BC-based materials through 3D printing or casting. easier comprehension because authors may use different acronyms for
It should be noted that in terms of generally accepted terminology, CBC the same substances. The list of abbreviations can be found at the end of
cannot be called a conductor, since the typical conductivity range of CBC the review.
hybrids lies in the semiconductor range (Solazzo et al., 2019). However, We begin with the main aspects of BC synthesis from the physico-
CBC is not a semiconductor because it lacks important properties of chemical point of view. We also discuss biosynthesis, chemical modifi
these materials. Therefore, we will follow the terminology accepted in cation, and vapor-phase polymerization as the main methods for pro
the BC-related literature and call the resulting hybrids “conductive”. ducing CBC. Then, we describe the main conductive components used to
Several reviews have been recently published about CBC (X. Chen create CBC: polyaniline, polypyrrole, PEDOT, other types of conductive
et al., 2016b; Y. Huang et al., 2021b; Mazhar Ul-Islam et al., 2021; polymers; graphene oxide, carbon nanotubes, nanoparticles, and metal-
Poddar & Dikshit, 2021). It is noteworthy that in this review, we provide organic frameworks. Next, tissue regeneration, drug delivery, elec
the most recent findings, focusing mainly on the applications of CBC trodes, supercapacitors, and aerogels are discussed as the main areas of
rather than on BC biosynthesis and processing. We also bring up several the current application of CBC. At the end of the review, we outline the
important issues with CBC development and discuss multiple possible main challenges associated with producing such composites and our
options for enhancing CBC advantages. We also mainly focus on modi ideas regarding further developments in this area.
fying BC without destroying its original form and maintaining the
Fig. 1. Scheme of BC formation. Bacteria synthesize linear cellulose molecules that are then combined into microfibrils. Both amorphous and crystalline regions are
present within the microfibrils. The microfibrils are then combined into macrofibrils, which are then combined into cellulose fibers.
2
2. BC production and properties in most studies (Esa et al., 2014; Reiniati et al., 2017). This strain pro
duces types I and II cellulose (Chawla et al., 2009). However, Agro
2.1. BC physico-chemical properties bacterium tumefaciens produces much shorter fibrils because it uses them
to attach to plants (Matthysse, 1983). Pseudomonas strains produce
The composition and the properties of BC have been well-studied thinner and more flexible fibrils (Deinema & Zevenhuizen, 1971). It
over the past few decades. However, they did not find ample applica should be noted that the BC of non-specific producer strains has not been
tion in science and technology. Occasionally, the investigation is per extensively studied. This is partly due to the low yield of BC and,
formed using a BC sample provided by fellow microbiologists. consequently, the economic inexpediency of strain cultivation. On the
Meanwhile, physico-chemical properties of initial BC can affect the other hand, it is possible to select optimal culture conditions for these
resulting composite quality, and namely, conductivity. Some physico- strains to ensure a high yield and obtain unique BC variants. Another
chemical features of BC will be outlined below. possibility to increase the yield and change the characteristics of BC is
Linear polymer chains of cellulose consist of subunits of one of the genetic modification of the strains. Various approaches can be found in
aqueous forms of glucose – β (1,4)-bound D-glucopyranosyl. Each reviews (Singh et al., 2020; Singhania et al., 2021).
monomeric unit is rotated by 180◦ with respect to the neighboring one
(Gopi et al., 2019). Such chains first form nanofibrils, which then 2.3. Effect of culture medium composition on BC properties
combine into microfibrils and finally into macrofibrils (Fig. 1) (Azeredo
et al., 2019). There are four types of cellulose (Thomas & Maria, 2016). The next aspect of BC production is culture medium composition.
Among them, nature cellulose (type I) consists of Iα and Iβ subtypes The yield of BC is very important from the commercial perspective. The
(allomorphs) (Ergun et al., 2015). They mainly differ in crystal struc yield depends on both the intrinsic characteristics of the strain and the
ture: Iα has a triclinic unit cell, while Iβ has a monoclinic unit cell. Most cultivation conditions and the culture medium. In general, the BC yield
of BC is classified as category Iα while plant cellulose mostly belongs to varies in the range of 1–10 g/L (Andriani et al., 2020). Glucose is the
Iβ (Yamamoto & Horii, 1993). Mercerization of BC is unavoidable to main source of nutrition, although a wide range of supplements can also
purify BC from bacteria and culture medium. It is an alkaline treatment be used (Chawla et al., 2009). A topic of particular ecological and eco
process (typically with NaOH) that changes crystalline structure from Iα nomic interest in this area is processing food production waste to obtain
type to II type. This conversion is irreversible; however, it can be BC (Hussain et al., 2019).
implemented in a controlled way to adjust BC strength characteristics In all cases, it is important for scientific research to precisely control
(Younesi et al., 2019). BC structural alterations after mercerization the composition of the culture medium. The standard medium for
involve changing from parallel orientation of BC (Iα) chains to an anti culturing A. xylinum is Hestrin-Scharmm (HS) medium (Esin Poyrazoğlu
parallel structure (II) (Kroon-Batenburg & Kroon, 1997). BC is also Çoban, 2011). Additives, such as carboxymethyl cellulose, can increase
called nanofibrillar cellulose because it has fibrils with diameters in the the yield of BC six-fold (Cheng et al., 2009). However, it should be noted
nanometer range. These structures have a high degree of crystallinity, that BC modified in this way loses much of its mechanical stability
which can be determined by XRD (Ruan et al., 2016). The process of (Young’s modulus decreases eight-fold). For some strains, maltitol is
fibril formation is possible because of the large number of hydroxyl more favorable for synthesis than glucose, leading to the yield increase
groups in the cellulose monomers involved in supramolecular forma (Singhsa et al., 2018). Ethanol is a common additive that increases the
tion. Besides, hydroxyl groups play a crucial role in the formation of BC yield (Krystynowicz et al., 2002). Gluconacetobacter sacchari was
bonds with the most conductive polymers, as shown in Section 3. used by Gomes et al. to study various substrates for bacterial growth
Adjustment of BC mechanical parameters can help to make it suitable (Gomes et al., 2013). They used dry olive mill residue as the main
for various applications. The principal mechanical properties of BC are substrate. However, overall, this substrate proved to be less profitable
as follows: elastic modulus ranging from 15 to 35 GPa, tensile strength than standard HS medium (0.85 vs 2.5 g/L yield). On the other hand,
ranging from 10 to 300 MPa, and elongation ranging from 1.5 to 2.0 % adding nitrogen and phosphate sources resulted in a 20–40 % increase in
(Gatenholm & Klemm, 2010). BC mechanical parameters appear to be the yield. Another important aspect of synthesis is the accumulation of
very different for the amorphous and crystalline parts of the microfibrils gluconic acid in the culture medium as the culture grows. This lowers
(Fig. 1). For crystalline domains, Young’s modulus can reach 130 GPa the pH and adversely affects the cultivation efficiency. Keshk and
(Retegi et al., 2010). introduction of various dopants into the BC Sameshima suggested adding lignosulfonate to the culture medium,
structure to change its conductive characteristics also changes its other which, under certain conditions, increased the yield by 57 % (Keshk &
characteristics, as shown below. Sameshima, 2006). A detailed review of the influence of the culture
There are several methods for changing the BC mechanical param medium on BC yield can be found in (Sperotto et al., 2021).
eters. NaOH treatment results in controlled changes in the tensile
strength in the range of 160–200 MPa (Suryanto et al., 2019) and in 2.4. Effect of culture conditions on BC properties
Young’s modulus in the range of 15–30 GPa (Nishi et al., 1990). The BC
strength is also dependent on its macrostructure, that is, the orderly Culture conditions affect both the yield and mechanical properties of
arrangement of fibrils. The formation of a honeycomb structure with BC. Bacteria can be cultured under static conditions or under stirring
polyvinyl alcohol doubles the strength of the BC to 315 MPa (Yu et al., (agitation). In the former case, a BC film is formed, which can be several
2020). However, this is not the limit for cellulose, and various post- centimeters thick, depending on the cultivation conditions (Hsieh et al.,
processing methods make it possible to obtain fibers with strengths up 2016). In the second cultivation method, various pellets appear; in
to 649 MPa (Q. Liang et al., 2021). general, their variety is reduced to scattered lumps of irregular or close
to rounded shapes (Aydın & Aksoy, 2014; Singhsa et al., 2018). The
2.2. BC-producing strains yield also depends on the cultivation method. For each strain, the
dependence of yield on agitation is different (Gao et al., 2020; Singhsa
Currently, there are at least 30 BC-producing strains (G. Li et al., et al., 2018). In addition, Singhsa et al. drew attention to the fact that
2022). They produce fibrillar cellulose with different structures. A stirring can increase the chance of mutant strains formed with a low BC
typical fibril diameter is 20–100 nm with a length of up to several mi yield (Singhsa et al., 2018). Stirring also significantly affects the pore
crons (Trache et al., 2020). However, different strains can produce size, making BC much more porous (Gao et al., 2020; Singhsa et al.,
completely different BC micromorphologies. Typical cellulose- 2018). This can affect the biodegradation degree, water retention, and
producing strains are Acetobacter xylinum, also known as Gluconaceto mechanical properties. It is also worth noting that small clumps of BC
bacter xylinus or Komagataeibacter xylinus, whose cellulose has been used resulting from agitation can serve as a ready scaffold for various
3
purposes, whereas the BC film needs to be processed to form a required under agitated conditions to form BC spheroids. Lv et al. used plain
shape. Another property that is affected by agitation is the crystallinity addition of multi-walled carbon nanotubes (MWCNTs) to the culture
of cellulose. This has been shown to decrease in agitated cultures (Gao medium to obtain a fuel cell electrode (Lv et al., 2016). Park et al. added
et al., 2020; Singhsa et al., 2018). The authors attributed this to me polymer-stabilized magnetic nanoparticles (NPs) to the culture medium
chanical interference during the crystallization. and obtained a magnetic composite (Park et al., 2013). In conclusion, it
can be said that biosynthesis is most often used to incorporate non-toxic
3. Methods for the CBC synthesis NPs into BC. Furthermore, we assume that its opportunities are much
wider, and additional research in this direction could simplify the pro
3.1. Biosynthesis of CBC cedure for obtaining CBC in one step.
Biosynthesis implies direct production of CBC during the bacteria

3.2. CBC synthesis via vapor phase polymerization
cultivation in a medium with a conductive component added (Fig. 2a).
The main requirements for the conductive component are its non-
Vapor phase polymerization (VPP) is commonly used to prepare BC
toxicity and minimal interaction with the culture medium compo
composites with polypyrrole (PPy). In a typical procedure, BC is soaked
nents. For instance, it should not oxidize the medium components or
in an iron (III) chloride solution and then saturated with pyrrole (Py)
result in any major pH change. This biosynthesis method has been
vapor under various conditions (Fig. 2b). A detailed analysis of the Py
shown to create ionistors when using graphene oxide (GO) (F. Guan
polymerization mechanism can be found in (Tan & Ghandi, 2013). PPy
et al., 2019). For this purpose, GO was added to the medium in the
is normally uniformly distributed on the surface of BC fibrils after
presence of polyvinylpyrrolidone (PVP). This led to the formation of a
polymerization, resulting in an increase in their diameter and their
3D honeycomb structure owing to the hydrogen bonds between GO and
partial aggregation (Fig. 4A). This causes some changes in mechanical
BC. A similar approach has been adopted by Liu et al. (K. K. Liu et al.,
characteristics. After coating with PPy, the pore volume of BC decreases
2018). Besides GO, SnO2 NPs were incorporated into the BC structure.
by at least 1.5 times (Yin et al., 2022). On the other hand, the tensile
After the BC/GO/SnO2 composite was obtained, a poly(3,4-
strength is increased by a factor of 2.5, which results from the rein
ethylenedioxyiophene)-poly(styrenesulfonate) (PEDOT:PSS) mixture
forcement of BC fibrils by PPy. Kwon et al. proposed the VPP method for
was added. Nandgaonkar et al. demonstrated an elegant method for the
creating a BC/PEDOT hybrid (Kwon et al., 2021). The BC was incubated
biosynthesis of BC/GO (Nandgaonkar et al., 2014). They used the ability
in a solution of oxidizing agents (iron (III) tosylate and pyridine) and
of yeast extract, one of the components of the culture medium, to act as a
then placed in the EDOT vapor atmosphere. Various research has shown
reducing agent for GO. GO was reduced in an autoclave during sterili
that the VPP method makes it possible to obtain thinner coatings on
zation of culture medium. Gluconacetobacter xylinus was then cultivated
substrates as well as longer and more orderly polymer chains (D’Arcy
Fig. 2. Methods for obtaining CBC. (a) Biosynthesis with addition of a conductive component to the culture medium. The conductive component is then embedded in
the growing BC film. (b) Vapor phase polymerization. The BC film is impregnated with a polymerization initiator solution and then placed in monomer vapor.
Polymerization occurs throughout the volume of BC with EC polymer-covered fibrils being formed. (c) Formation of conductive layers. A culture medium containing
a conductive component is stepwise applied to the surface of growing BC. As a result, layer-by-layer structure with alternating conductive and dielectric layers is
formed. (d) Chemical modification of BC. BC is impregnated with monomer solutions, which is further polymerized with an initiator solution. (e) Synthesis of NPs
inside BC. BC is modified with a precursor solution, after which NPs are synthesized on fibrils using various methods. (f) Formation of conductive materials by casting
or printing. BC film is homogenized, and a gel-like material is prepared, which can be poured into molds or printed together with a conductive component.
4
et al., 2014; J. Kim et al., 2003). This can result in a higher conductivity readily owing to polymer water solubility. In this case, BC can be simply
of such polymers as PPy and PEDOT. soaked in PEDOT:PSS solution and dried (Fig. 4C) (S. Khan, Ul-Islam,
Khattak, Ullah, Park, 2015a).
3.3. Formation of CBC with conductive layers
3.5. CBC fabrication via synthesis of NPs within BC structure
To create conductive interfaces or electrodes, it is sometimes
necessary to provide selective volume modification of BC where some The synthesis of NPs directly within the BC film enables forming
areas remain dielectric. Shi et al. developed a BC surface modification homogeneously distributed NPs with specific parameters. An important
approach by polymerization of conductive polymer with a couple of flat aspect is the pretreatment of BC films with the reagents that would act as
electrodes (Z. Shi et al., 2014). Moreover, owing to its resistance, the nucleation points for NPs and ensure their bonding with the fibrils
main layer of BC can act as an insulator, separating the two conductive (Fig. 2d). Zhang et al. used polydopamine (PDA) for this purpose (L.
layers on both sides. The middle layer can also be doped with an Zhang et al., 2021). PDA is known for its high affinity to many metals (Y.
appropriate substance to give BC the properties of ion conductivity. Lin Liu et al., 2014). PDA-coated BC/GO was soaked in silver nitrate and
et al. proposed a different mechanism for creating a conducting layer on irradiated with UV light to reduce Ag and form Ag NPs (L. Zhang et al.,
the BC surface (Lin et al., 2013). The BC film was placed on the interface 2021). Gutierrez et al. reported the possibility of incorporating vana
between the aniline solution in toluene and APS. Thus, aniline poly dium oxide NPs into the BC structure by in situ sol-gel synthesis from
merization occurred only on the surface layers of BC. The measurements vanadium (V) oxytriisopropoxide, isopropanol, and hydrochloric acid
indicated that the resistance of the conducting side was approximately (Gutierrez, Fernandes, Mondragon, and Tercjak, 2012a). Li et al. fabri
40 Ω × cm. The unmodified side had a resistance of 108 Ω × cm, which cated a composite of BC and Pd NPs (D. Li et al., 2016). To achieve this,
did not differ from that of the initial BC. Another approach has been homogenized BC without any additional chemical modifications was
proposed in some articles, including those by Wan et al. (Wan et al., mixed with PdCl2, which was reduced with K[BH4]. According to TEM
2021). It combines biosynthesis approaches and the formation of a images, the Pd NPs were evenly distributed on the BC fibrils. The pro
necessary conducting layer. This involves creating a film of conventional duction of various MOFs within BC structures has also been reported.
BC and then applying a culture medium containing a dopant (Fig. 2c). Huang et al. performed BC chelation with Co(NO3)2 ⋅ 6H2O to produce
Wan et al. used Ti3C2Tx MXenes. This results in a composite containing the Co-containing MOF ZiF-67 (Q. Huang et al., 2021a). ZiF-67 was
2D particles that are built layer-by-layer into the BC structure. An prepared by adding Hmim (C4H6N2) as a reducing agent to the cobalt
interesting approach for printing layers on the surface of BC was pro nitrate-treated BC. A similar method, using Zn(NO3)2 ⋅ 6H2O, was used
posed by Avila et al. (Avila et al., 2018). Poly (phenylene vinylene) to obtain BC/ZiF-8 (S. Zhang, Luo, Zhang, Du, Hui, Zhao, He, and Sun,
(PPV) films were deposited on the BC surface using laser-induced for 2022b). In both cases, the reaction was carried out in anhydrous
ward transfer. The accuracy of the method is approximately 10–20 μm, methanol.
which provides electrically conductive tracks and even microcircuits on
the surface of the BC. 3.6. Approaches to the formation of conductive 3D BC-based composites
3.4. CBC synthesis via chemical modification Most BC-based composites inherit the shape of the original BC film. It
is possible to grow BC in test tubes of a certain size or cut a BC film into
Chemical modification in solution is considered the most common pieces of the desired size. However, this does not result in complex 3D
method for CBC production. Generally, it involves soaking the BC film structures. For that, it is necessary to use 3D printing, casting, extrusion,
under various conditions in a solution of monomers. Monomers can be or other techniques. For the above, BC must be dissolved using adequate
polymerized throughout the BC using chemical agents (Fig. 2d). CBC methods, and bioink suitable for printing has to be synthesized. Since in
composites with polyaniline (PAni) and PPy are usually fabricated by this review we focus on the inherent fibrillar structure of BC (which is
this method. BC/PAni was obtained from aniline hydrochloride by inevitably destroyed during the BC gel formation), we will discuss only a
adding ammonium peroxodisulfate (Z. Shi et al., 2012). This method few approaches to the formation of conductive materials by printing
produces a coating on the surface of BC fibrils, which is very similar to methods.
that of PPy (Fig. 4B). This changes the mechanical characteristics as well The main advantage of printing with BC-based conductive gels is the
as the BC surface chemistry. For example, Hu et al. showed that the possibility to produce samples with desirable geometry and properties.
tensile strength of BC/PAni decreases 3.5 times (Hu et al., 2011). The Fabrication of CBC within this approach involves 3D modelling using
authors explained this by a decrease in the number of hydrogen groups computer software; ink preparation; optimizing printing parameters and
due to coating fibrils with a layer of PAni. It is also possible to obtain BC/ direct printing with inks onto the printer platform (Fig. 2f) (Vidakis
PAni using iron (III) chloride as an oxidizing agent (Marins et al., 2014). et al., 2021). Depositing PEDOT:PSS as a conductive polymer on the BC
Another pathway of PAni synthesis is the oxidation of aniline by laccase surface provides a composite with enhanced effective area of the elec
(Shim, Noro, Cavaco-Paulo, Silva, and Kim, 2019a). However, some trical double layer of PEDOT:PSS as reported by Inácio et al. (Inácio
additional agents are required, for example, the radical initiator potas et al., 2020). The upper layer of BC fibers was impregnated with PEDOT:
sium hexacyanoferrate (II) trihydrate (KHCF) and the surfactant bis PSS ink which resulted in an enhanced electrode active area. There is
(2–ethyl hexyl) sulfosuccinate (AOT). Added together, they allow to also an opportunity to produce CBC with inorganic electroconductive
produce BC with a conductivity of about 7 × 10-4 S/cm, while without compounds. Pedrotty et al. developed 3D conductive biopatches by
them it is of ca. 0.3 × 10-4 S/cm. Shim et al. used 1-Hydroxybenzotria using printable BC/CNTs ink (Pedrotty et al., 2019). CNTs and nano
zole (HBT) as an aniline polymerization mediator and received con fibrillated BC solution were mixed and the resulting ink was loaded to
ductivity values of ca. 9 × 10-4 S/cm (Shim, Su, Noro, Teixeira, Cavaco- the printer nozzle to fabricate a patch.
Paulo, Silva, and Kim, 2019b). Gadim et al. proposed the polymerization
of sodium 4-styrenesulfonate (NASS) using PEGDA to create an ion- 4. Materials for CBC fabrication
conductive composite (Gadim et al., 2014). As a result, the fibrils
were covered with a layer of PSS, and the number of sulfonic acid groups 4.1. Polypyrrole
was controlled by the concentration of PEGDA. This study focused on the
change in CBC conductivity under different humidity values. Overall, Polypyrrole (usually designated as PPy) is a product of oxidative
the maximum conductivity was relatively high, 0.1 S/cm. When a polymerization of pyrrole (Fig. 3). Its conductivity has been reported for
polymer mixture of PEDOT:PSS is used, CBC can be obtained more over a century and it is widely used in biology, medicine, and electronics
5
Fig. 3. Chemical structure of the main compounds used to create CBC.
(Z. B. Huang et al., 2014; Jain et al., 2017; Zare et al., 2021). The con supercapacitors. The main advantage of the electrochemical oxidation
ductivity of PPy depends on its oxidation state (Pang et al., 2021). In the method is the increase in the capacitance of PPy, which is essential for
undoped state, it acts as an insulator, whereas in the doped state, it is a fabricating ionistors (Wolfart et al., 2016). This phenomenon is related
conductor. However, in the oxidized state, it becomes black and opaque to the “adequate” ratio of oxidized and non-oxidized PPy chain
(as do BC/PPy composites). This can be considered a disadvantage, fragments.
especially when composites are intended for use in optical-related areas.
Oxidation of Py usually occurs under the action of iron (III) oxide or 4.2. Polyaniline
ammonium persulfate (APS) under various conditions (typically at low
pH). Acidic pH can result in a degradation of BC fibrils and a loss of Polyaniline (PAni) is a derivative of the simplest aromatic amine
mechanical properties of the BC/PPy composite obtained (Beneventi aniline. PAni has been known for two centuries and it is one of the most
et al., 2006). Besides, different oxidizing agents yield different con well studied conductive polymers. This made PAni one of the first
ductivity values, even at the same concentrations of PPy (Muller et al., modifiers used to fabricate CBC. Its obvious disadvantages include the
2013). At a PPy concentration of 0.01 M, the conductivities of the BC/ black color and opacity of the resulting samples. There was also a sig
PPy/APS and BC/PPy/FeCl3 composites were 7.8 × 10-7 and 3.7 × 10-7 nificant decrease registered in the ability of BC to retain water, which
S/cm, respectively. It is also worth mentioning that Young’s modulus for was associated with PAni hydrophobicity (Alonso et al., 2018; Shim, Su,
BC/PPy/FeCl3 was approximately 7–15 times lower than that of the Noro, Teixeira, Cavaco-Paulo, Silva, and Kim, 2019b). The BC/PAni
initial BC, whereas for BC/PPy/APS, it was only 2–3 times lower. This is complex is formed due to the dehydration–condensation reaction and
consistent with the theory that rapid and uncontrolled oxidation can the formation of hydrogen bonds (Z. Shi et al., 2012). During aniline
damage the BC fibrils. To control the oxidation rate, temperature can be polymerization, NPs (Antonel et al., 2015; Eftekhari & Afshani, 2006) or
lowered along with varying the time and/or concentration of the metals (H. Kim et al., 2020) can be incorporated into the PAni structure.
oxidizer (J. Xu et al., 2013). For example, Xu et al. achieved a conduc The conductive characteristics of BC/PAni are highly dependent on the
tivity of 3.9 S/cm by optimizing the CBC synthesis process using FeCl3 as structure of the polymerized PAni. The latter exists in three states: leu
the oxidizing agent (J. Xu et al., 2013). coemeraldine, emeraldine, and (per)nigraniline (Masters et al., 1991).
PPy is often used in combination with other conductive dopants, for The first and the third states are the fully reduced and fully oxidized
example, GO. In the latter case, the conductivity of the resulting com states of PAni, respectively. Both are considered poor conductors.
posites exceeded that of each component (Y. Liu et al., 2015). Liu et al. Emeraldine (or emeraldine base, EB) forms an emeraldine salt (ES) upon
prepared several types of BC, BC/GO, and BC/PPy composites and protonation. ES is considered the most useful form of PAni because it
investigated GO and PPy separately (Y. Liu et al., 2015). It is BC/PPy/ possesses the highest degree of conductivity. Therefore, the polymeri
GO composite that showed the highest conductivity of 13.2 S/cm; GO zation of aniline within BC structure has to continue for a specific time to
had 0.54 S/cm, BC/GO had 1.71 S/m, and PPy had 1.07 S/cm, respec ensure the proper degree of aniline oxidation. For example, Shi et al.
tively. The authors attributed this to the fact that BC structure helps to showed that polymerization for 30 min resulted in the highest conduc
enhance conductivity by means of numerous conducting fibrils acting as tivity (1.3 × 10-2 S/cm), while doubling this time resulted in a decrease
wires. At high PPy concentrations, conductivity decreases, which results in conductivity (4.5 × 10-3 S/cm). The highest possible conductivity
from a strong alteration in the internal structure of BC (disturbance of obtained was 10-1 S/cm when BC/PAni composite was acid-doped (Z.
the fibrillar network) (Y. Liu et al., 2015). Shi et al., 2012). Yue et al. used the same approach but with carbox
Some polymerization methods using peroxydisulfates and electro ymethylated BC, which allowed them to obtain the conductivity values
chemical oxidation have been developed. For example, Bai et al. used of up to 1.7 × 10-2 S/cm (Yue et al., 2016). Hu et al. obtained values of
electrochemical oxidation to develop a BC/rGO/CNTs/PPy composite. up to 5 × 10-2 S/cm (Hu et al., 2011). On the other hand, there was a
This composite was successfully used as an electrode for decrease in the tensile strength of BC observed. A 3-fold decrease in
6
tensile strength was also reported by Lin et al. (Lin et al., 2013). Alonso hydrophilic BC and mechanically strong PPTA results in separators with
et al. conducted a comprehensive study on the effects of the methods for enhanced electrical properties. The ionic conductivity of the resulting
preparing the initial BC (drying, freeze-drying, and draining) on the final membrane was approximately 12 × 10-3 S/cm, and the strength was
composite parameters (Alonso et al., 2018). They found that composites 104.7 MPa (2.5 times greater than that of BC). Zhu et al. used poly
parameters are very different and can be used for different purposes. For phenylene sulfide (PPS) to obtain a separator for LIB (C. Zhu et al.,
example, the composite obtained from freeze-dried BC had the highest 2021). They achieved an ionic conductivity of 1.55 × 10-3 S/cm, which
hydrophilicity, while drained BC made it possible to obtain a composite was five times higher than that of a Celgard 2400 separator. However, it
with the highest conductivity of up to 1.4 × 10-1 S/cm. Fei et al. pro should be noted that BC was homogenized and pressed to obtain the
posed modifying BC with epoxy chloropropane to improve the interac final composite, that is, the original BC structure was destroyed (Fig. 2f).
tion of BC with PAni, and then introduced polyacrylamide to improve Aleshin et al. developed light-emitting paper based on BC using the
the strength characteristics of the composite (Fei et al., 2019). This MEH-PPV polymer (Aleshin et al., 2017). The BC was immersed for 15 h
resulted in both an increase in the conductivity from 1.24 to 1.43 S/cm in a polymer solution in chloroform and then dried. For electrolumi
and in improved tensile strength from 18.97 to 47.94 MPa. Numerous nescence, the composite was placed between two silver electrodes, and
researchers have used the oxidation of aniline with laccase as an envi voltages in the range of 20–50 V were applied. Jiajia et al. used poly
ronmentally friendly synthesis method. However, the conductivity indole as a conductive polymer to fabricate BC-based electrodes (Jiajia
values of the CBC have been shown to be considerably lower compared et al., 2020). The composite also contained CNTs and D-tartaric acid as
to iron (III) chloride oxidation. For example, Shim et al. obtained values dopants. The electrodes were produced by electrospinning, which
of approximately 5.5 × 10-4 S/cm and improved them to 8.5 × 10-4 S/cm destroyed the original BC structure.
using ultrasonic treatment of the composite (Shim, Su, Noro, Teixeira,
Cavaco-Paulo, Silva, and Kim, 2019b). 4.5. Nanomaterials
4.3. PEDOT:PSS Metals and their oxides are the most obvious options for conductive
dopants in BC. However, their incorporation into the internal structure
Poly(3,4-ethylenedioxythiophene) (PEDOT) is a widely used of BC is challenging. Nanomaterials (NMs) are reported to have been
conductive polymer (Groenendaal et al., 2000). PEDOT is insoluble in used to overcome these issues. Many NMs are known to conduct elec
water; however, if it is synthesized in the presence of polystyrene sul tricity. Owing to their size, they can be embedded in the BC pores, thus
fonate (PSS), there is aqueous dispersion obtained (Wen & Xu, 2017). providing conductive properties.
Therefore, the combination of PEDOT:PSS is often used. Polycationic Carbon nanotubes (CNTs) have been known for >30 years and are
PEDOT chains are included in the PSS polyanionic matrix for charge widely used for electrically conductive modifications. Their properties
compensation. When doped with PSS, PEDOT acquires p-type conduc have been amply reviewed (Anzar et al., 2020; Gupta et al., 2019). The
tivity and can be used to produce electrodes (Kuş & Okur, 2009). One of obvious disadvantages of using CNTs include the same black color and
the main differences between PEDOT:PSS and PAni/PPy is the trans opacity of the resulting composites as those when using PAni or PPy.
parency of the former in the visible region of the spectrum. This presents Moreover, CNTs have different types of toxicity, although they are
wide opportunities for both electrical- and light-conducting structures generally considered as low-toxic NMs (Mohanta et al., 2019). Another
(C. Chen et al., 2015). An additional inclusion of NPs in the PEDOT:PSS disadvantage of these materials is their hydrophobicity. Incorporating
structure significantly expands its opportunities. Liu et al. demonstrated them into hydrophilic BC requires polar solvents or surfactants. One of
that BC can be impregnated with PEDOT:PSS, and adding tin oxide and the most common surfactants is CTAB, which is known to be toxic and
rGO NPs produces an efficient ionistor (K. K. Liu et al., 2018). Khan et al. mutagenic (Golubev et al., 2016). It is poorly washed during cyclic
reported fabricating a CBC with a high conductivity of 12.17 S/cm by washing and exhibits toxicity, even at low trace concentrations (Boga
using only PEDOT:PSS. However, the amount of incorporated polymer tyrev et al., 2015). The conductivity of the CBC with incorporated CNTs
reached 31.24 wt% (S. Khan, Ul-Islam, Khattak, Ullah, Park, 2015a). varied within 1–3 × 10-2 S/cm (Fig. 4E) (Yoon et al., 2006).
Kwon et al. suggested using VPP to produce BC/PEDOT composites Au, TiO2, ZnO, SnO2, and many other NPs have been used to produce
(Kwon et al., 2021). They obtained a record conductivity of approxi CBC. Multicomponent electrodes were fabricated by simultaneously
mately 278 S/cm. The final conductivity was affected by many param including CNTs and gold nanoparticles (Au NPs) within BC structure (Lv,
eters, including oxidant concentration and reaction time. The authors Zhou, Mensah, Feng, Wang, Hu, Cai, Amerigo Lucia, Li, and Wei,
believe that the key to obtaining composites with such high conductivity 2018a). While the CNTs provided conductivity, the AuNPs acted as
is the slow polymerization of EDOT from the gas phase, which makes it conductors for the enzymes included in the electrode structure. This
possible to create more ordered structures. Besides, VPP resulted in resulted in the formation of a self-powered biosensor for glucose
mechanically stronger samples. The tensile strength of VPP-produced detection. Notably, the growth of AuNPs occurred in situ on the modi
BC/PEDOT composite was 45 MPa while solution polymerization- fied CBC. They were evenly distributed over the surface of the CBC;
produced BC/PEDOT composite provided only 20 MPa. There are however, there was no volumetric distribution measurement provided.
more examples of BC/PEDOT in the sections to follow, as PEDOT is TiO2 NPs has also been reported as dopants for CBC (Gutierrez, Tercjak,
found to be the most suitable for various biomedical applications. Algar, Retegi, and Mondragon, 2012b). However, the conductive
behavior of the obtained hybrid was only shown by electrostatic force
4.4. Other conductive polymers microscopy, and no quantitative information (in terms of S/cm) was
provided. The same group of researchers proposed a method for the
Among other polymers used to produce CBC, the derivatives of poly synthesis of CBC using vanadium oxide NPs (Gutierrez, Fernandes,
(p-phenylene) and polyphenylene are worth discussing. Poly (p-phe Mondragon, and Tercjak, 2012a). A distinctive feature of this composite
nylene terephthalamide) (PPTA) is also known as aramid. PPTA forms was the photoresponsive behavior resulting from the changing color and
hydrogen bonds with other polymers (Y. Guan et al., 2017); thus, the transparency. Pirsa et al. used ZnO NPs in combination with PPy (Pirsa
BC/PPTA composite can be easily obtained (Y. Yang et al., 2020). et al., 2018). Hydrophobicity of PPy reduces the ability of BC to retain
Aramid is widely used as a separator for lithium-ion batteries (LIB). water, which is compensated for by the hydrophilicity of ZnO. On the
Unmodified BC can also be used as a separator for LIB with minimal other hand, ZnO reduces conductivity. SnO2 has also been used in
treatment. However, owing to the presence of multiple hydrogen bonds, combination with PPy (Fig. 4F) (Ye et al., 2019). The inclusion of SnO2
its efficiency is low (Q. Huang & Zhao, 2021). This requires an addi NPs increased the conductivity from 1.152 S/cm (BC/PPy) to 7.246 S/
tional increase in its mechanical stability. The combination of cm (BC/PPy/SnO2). Park et al. created a magnetic BC composite using
7
Fig. 4. SEM images of CBC obtained by different methods. (A) CBC prepared with PPy via polymerization with iron (III) chloride. Reprinted from (J. Xu et al., 2013)
with permission from Elsevier. (B) CBC prepared with PAni via polymerization with APS in solution. Reprinted from (Z. Shi et al., 2012) with permission from The
Royal Society of Chemistry. (C) CBC prepared from PEDOT:PSS by immersion in an aqueous solution of PEDOT:PSS. Reprinted from (S. Khan, Ul-Islam, Khattak,
Ullah, Park, 2015a) with permission from Elsevier. (D) CBC prepared using GO and loaded with ibuprofen. The red arrows indicate ibuprofen, and the yellow arrows
indicate GO. Reprinted from (Luo et al., 2017) with permission from Elsevier. (E) CBC with MWCNTs. Reprinted with permission from (Yoon et al., 2006). Copyright
2006 American Chemical Society. (F) CBC composed of SnO2 NPs and PPy. Reprinted from (Ye et al., 2019) with permission from Elsevier. (For interpretation of the
references to color in this figure legend, the reader is referred to the web version of this article.)
magnetite NPs (MNPs) and PAni (Park et al., 2013). A high conductivity conductivity of BC.
of 0.31 S/cm was provided by PAni, but including MNPs increased it up
to 0.43 S/cm. The authors attributed this to the compaction of the CBC
structure and an increase in the number of contacts between the fibrils. 4.6. Graphene oxide
Silver and copper are metals with some of the highest conductivities.
However, there are only a few examples of BC composites incorporating BC is widely used in combination with GO. Owing to the strong van
them. The addition of copper (II) sulfate to BC/PAni increased its con der Waals interactions, GO tends to agglomerate in the dried state,
ductivity 3.8 times up to 7.54 × 10-2 S/cm (H. Kim et al., 2020). How which is adverse for its properties (C. Li et al., 2017). BC is an excellent
ever, it is essential that many metal salts can act as oxidizing agents, scaffold for maintaining the GO in dispersed state. Because of the large
which results in excessive oxidation of PAni and a decrease in its con number of hydrophilic hydroxyl groups in both the materials, they
ductivity, according to the above authors. Lv et al. used Ag nanowires to readily form hydrogen bonds. GO is also well dispersible in water, and
create a conductive transparent composite (Lv, Zhou, Zhao, Li, Lu, BC is highly hydrophilic, which ensures good BC pore filling (Si, Luo,
Wang, Huang, Cai, Lucia, and Wei, 2018b). The resistance of the Xiong, Yang, et al., 2014a). BC/GO can be used for fabricating super
resulting film was approximately 7.5 Ω/sq. Zhang et al. used magnetron capacitors (F. Guan et al., 2019), for improving BC mechanical param
sputtering to create a silver film on the surface of BC to fabricate a eters (Luo, Dong, Yao, Yang, Li, Wang, Xu, Hu, and Wan, 2018a), and for
surface-enhanced Raman scattering (SERS) substrate (S. Zhang, Xu, Liu, designing drug delivery systems (Fig. 4D) (Luo et al., 2017). GO is
Huang, and Jiang, 2022c). Specific conductivity values were not known to be a poor electrical conductor unless it is reduced by heating
measured. (Jakhar et al., 2020) or chemical agents (Chua & Pumera, 2014). The
There were several studies of incorporating metal-organic frame inclusion of GO can significantly increase the BC conductivity. However,
works (MOFs) into BC structure. MOFs feature porosity among other GO is a poor electrical conductor. To give it electrically conductive
advantageous properties. Combined with the BC porosity, this produces properties, it is reduced by heating (Jakhar et al., 2020) or chemical
unique composites. Huang et al. applied this method to create separators agents (Chua & Pumera, 2014). Guan et al. showed that the conductivity
for LIB and noted the excellent electrolyte retention capacity and of BC/holey GO composite is about 1.15–2.83 S/cm (F. Guan et al.,
wettability of the BC/ZiF-67 composite (Q. Huang et al., 2021a). Owing 2019). Ccorahua et al. treated BC/GO composites with hydrazine vapor
to these properties, the ionic conductivity increased 6.5 times to 0.837 to reduce GO to rGO and increased the conductivity six-fold (Ccorahua
× 10-3 S/cm. A similar synthesis method proposed by Zhang et al. et al., 2017). If such composites are doped with NH4I, an ionic con
resulted in ionic conductivity of 1.60 × 10-3 S/cm (S. Zhang, Luo, Zhang, ductivity of 10-4 S/cm can be achieved (Torres et al., 2019). Including
Du, Hui, Zhao, He, and Sun, 2022b). In their work, they used MOF ZiF-8 any NMs in the BC structure is also known to change its mechanical
together with aramid fibers. This resulted in doubling the ionic characteristics. For GO, a 2–3-fold increase in the tensile strength was
observed compared to that of unmodified BC (F. Guan et al., 2019).
8
Another study reported an increase in strength of 38 % (Si, Luo, Xiong, 5. Selected CBC applications
Yang, et al., 2014b).
Some of the above examples of CBC composites are summarized in 5.1. Drug delivery
Table 1.
CBC can be used for the controlled release of drugs through ionto
phoresis (Kalia et al., 2004). For plant cellulose, a positive effect of
iontophoresis was observed for buprenorphine (Fang et al., 2010).
Table 1 Owing to the similarity in their chemical structures, a comparable effect
CBC examples, their conductivity and applications. can be achieved using BC. Drugs can also be released from the scaffold at
Conductive Conductivity, Applicationb Ref. a certain pH. The natural ability of BC to retain up to 1000 % water by
additive S/cma weight makes it a promising option for prolonged release. Li et al.
PAni 7 × 10-4 Enhanced (Shim, Noro, Cavaco- showed that a multilayer BC/PAni composite has different abilities to
conductivity Paulo, Silva, and Kim, release drugs at acidic and alkaline pH (S. Li et al., 2018). This phe
2019a)
nomenon was attributed to the surface-charged CBC layer in the pro
PAni 9 × 10-4 Enhanced (Shim, Su, Noro,
conductivity Teixeira, Cavaco- tonated state at a low pH, which acts as a natural barrier for charged
Paulo, Silva, and Kim, drug molecules. The load is released with pH increase. Shi et al. com
2019b) bined the two modalities of pH-dependent and electrically stimulated
PSSA 10-1 Membranes for fuel (Gadim et al., 2014) release (X. Shi, Zheng, Wang, Yue, Qiao, Wang, Wang, and Quan,
cells and batteries
PPy 3.7 × 10-3 Enhanced (Muller et al., 2013)
2015b). They developed a hydrogel comprising BC, sodium alginate,
conductivity and MWCNTs. Under alkaline pH, the release of ibuprofen was much
PPy 3.9 Supercapacitor (J. Xu et al., 2013) higher than that in the acidic environment (~ 90 % vs. 30 %). On the
electrode other hand, there was no difference in the release with or without an
PPy/GO 13.2 Supercapacitor (Y. Liu et al., 2015)
electrical stimulus whether at acidic or alkaline pH values. However, at
electrode
GO 5.4 × 10-1 Supercapacitor (Y. Liu et al., 2015) neutral pH a significant increase in the release was observed under the
electrode pulsatile action of the electric field (Fig. 5A). This presents an oppor
PPy 1.07 Supercapacitor (Y. Liu et al., 2015) tunity for a dual-purpose drug depot (Krathumkhet, Imae, Paradee,
electrode 2021b). A similar drug release system was suggested by Krathumkhet
-2 -1
PAni 1.3 × 10 –10 Enhanced (Z. Shi et al., 2012)
conductivity
et al. (Krathumkhet, Imae, Paradee, 2021a). They also studied the
PAni 1.7 × 10-2 Enhanced (Yue et al., 2016) release of ibuprofen and showed a similar dependence of the release on
conductivity the pH and electric field. Chen et al. proposed another method for
PAni 3 × 10-4–5 × Enhanced (Hu et al., 2011) creating microfibers from BC with controlled drug release (C. Chen
10-2 conductivity
et al., 2017). They fabricated a microfiber from BC with a diameter of
PAni 1.4 × 10-1 Enhanced (Alonso et al., 2018)
conductivity 100 μm surrounded by a thin shell of PEDOT. Under the electric field,
PAni 1.43 Conductive paper (Fei et al., 2019) PEDOT mechanically contracts, resulting in the release of the load
PEDOT:PSS 12.17 Optoelectronic (S. Khan, Ul-Islam, (diclofenac sodium) from the CBC. The composite was also highly
applications Khattak, Ullah, Park, biocompatible (Fig. 5B).
2015a)
PEDOT 278 Flexible film (Kwon et al., 2021)
PPTA 12 × 10-3 LIB separator (Y. Yang et al., 2020) 5.2. Tissue regeneration and wound healing
PPS 1.55 × 10-3 LIB separator (C. Zhu et al., 2021)
MWCNTs 1.4 × 10-1 Enhanced (Yoon et al., 2006) Body tissues differ considerably in their ability to regenerate. Tissues
conductivity
that lack complex cellular organization, such as skin, regenerate more
SWCNTs 0.95 Myocardium (Pedrotty et al., 2019)
treatment actively, while cartilage, cardiac, and the central nervous system do not
PPy/SnO2 7.246 Enhanced (Ye et al., 2019) regenerate because of a limited supply of endogenous cells (Gaharwar
conductivity et al., 2020). Most tissue engineering approaches for poorly regenerating
-1
PAni/MNPs 4.3 × 10 Magnetic composite (Park et al., 2013) tissues require using various microporous, fibrillar, nanostructured or
PAni/copper 7.54 × 10-2 Enhanced (H. Kim et al., 2020)
sulphate conductivity
other scaffolds to anchor the cells within them (Gaharwar et al., 2020).
ZiF-67 0.837 × 10-3 LIB separator (Q. Huang et al., Various gels based on gelatin, sodium alginate, chitosan, silk, hyaluronic
2021a) acid, and polymers, such as polypropylene, polycaprolactone, and
-3
ZiF-8 1.60 × 10 LIB separator (S. Zhang, Luo, PLGA, are widely used as scaffold biomaterials. The main parameters
Zhang, Du, Hui, Zhao,
affecting scaffold biocompatibility are surface chemistry (type of func
He, and Sun, 2022b)
GO 1.15–2.83 Supercapacitor (F. Guan et al., 2019) tional groups, surface charge, and hydrophilicity/hydrophobicity) and
electrode physical structure (size, amount, and shape of pores, stiffness, tensile
GO 10-4 Enhanced (Torres et al., 2019) strength, and elasticity). Some parameters are crucial for cell adhesion
conductivity within scaffolds.
-2
PVP/PVA 3.4 × 10 Enhanced (Guo, Yuan, Huang,
conductivity Zhang, et al., 2022a)
Porosity is one of the important parameters above. Porosity increases
PEDOT 7.3 × 10 -2
Biomedical (S. Khan, Ul-Islam, scaffold permeability for macrophage infiltration and enhances the
application Khattak, Ullah, Park, growth of new vessels (Sussman et al., 2014). Non-porous scaffolds are
2015b) predominantly replaced by connective tissue, whereas porous scaffolds
MWCNTs 5.3 × 10-3 Conductive (Jung, Kim, Kim,
promote angiogenesis and extracellular matrix formation (Lutzweiler
transparent paper Kwon, et al., 2008a)
PEDOT:PSS 7 × 10 -1
Biocompatible (Vadanan & Lim, et al., 2020). Almost all hydrogels based on natural polymers can be
conductive foam 2022) transformed into porous structures by electrospinning, supercritical
MXene 156 EM shielding (Wan et al., 2021) drying, or 3D printing (Annabi et al., 2010). However, BC is much
a
Best value among other samples reported in the work. stronger compared to other polymer-based scaffolds. For example, it is
b
We use the notion “Enhanced conductivity” when research has dealt with the three times stronger than chitosan (Martins et al., 2014). Moreover, the
CBC conductive properties and their improvement without specifying the inherent porous structure of BC makes it easier to obtain scaffolds
application of the resulting composite. without extra processing.
9
Fig. 5. Selected applications of CBC. (A) Pulsatile release of a drug under electrical stimulation of the CBC. Reprinted from (X. Shi, Zheng, Wang, Yue, Qiao, Wang,
Wang, and Quan, 2015b) with permission from The Royal Society of Chemistry. (B) Cell alignment on BC/PEDOT under electrical stimulation. Cells were stained
with FITC-β-III-tubulin. Reprinted from (C. Chen et al., 2017) with permission from Elsevier. (C) Cells grown on BC/GO/PPy under electrical stimulation. Reprinted
with permission from (C. Chen et al., 2016a). Copyright 2016 American Chemical Society. (D) Flexible humidity sensor with BC/MXene/GO as the active component.
Reprinted from (Ge, Zeng, Hu, Yang, et al., 2022a) with permission from Elsevier. (E) Autonomous electromagnetic sensor based on BC/CoFe2O4. Reprinted from (K.
Chen, Li, Du, Hu, et al., 2022a) with permission from Elsevier. (F) Fully flexible LIB lithium-ion battery. Reprinted with permission from (Zhou, Liu, Du, Ren, et al.,
2019a). Copyright 2019 American Chemical Society.
Surface hydrophilicity is also important for biocompatibility since (Fig. 5C). The idea of using PEDOT as a conductive polymer relates to
cells better adhere to hydrophilic surfaces (H. Shi, Gan, Liu, Ma, Hu, the fact that the presence of a PEDOT layer on the BC surface can pro
Yuan, and Liu, 2015a; van Wachem et al., 1985). However, many other mote cell proliferation (S. Wang et al., 2018). The density of the cell
factors make hydrophilic surfaces preferable for tissue engineering and layer and cell viability were higher after cultivation on a PEDOT-
regeneration (Kasemo, 2002). For instance, hydrophilic surfaces better covered surface. It has also been shown that cells express significantly
adsorb albumin, which results in the release of anti-inflammatory cy more Ki67, a marker of proliferation. Liu et al. took a step further and
tokines by tissue macrophages and improves the graft survival rate conducted animal studies using BC/sulfonated PEDOT (G. Liu et al.,
(Visalakshan et al., 2019). As mentioned above, BC has a large number 2022). They showed that implanting a BC-based composite resulted in
of hydroxyl groups, making it a highly hydrophilic material. better tissue regeneration than without doing so. However, special
Thus, a combination of factors, such as porosity, hydrophilicity, non- studies on the dependence of the regeneration rate on the conductive
pyrogenicity, mechanical strength, and ease of fabrication, makes bac parameters of the composite do not seem to have not been provided yet.
terial cellulose a promising material for tissue engineering and More details on the approaches to neural tissue repair using BC can be
regeneration. found in a recent review (Jabbari et al., 2022).
Tissue regeneration using CBC can be achieved in several ways. First, Another effect of CBC is the regulation of drug release or physical
the conductive tissue (nerve or muscle) is replaced with BC-based grafts. effect on the surrounding tissues to stimulate regeneration. Electrical
It has been repeatedly shown that BC is similar to the extracellular stimulation has also been shown to accelerate wound healing (Long
matrix, which allows cells to be oriented and grow in a certain way et al., 2018). In some cases, the voltage applied was directly related to
(Svensson et al., 2005; Torgbo & Sukyai, 2018). Formation of tissue the rate of cell proliferation (Santos et al., 2017). From this perspective,
analogs with BC was mainly observed for the nervous tissue. Recently, a CBC may be an ideal option. Zhang et al. suggested using BC/GO/AgNPs
successful effect of unmodified BC on the ability to regenerate nervous as wound dressings (L. Zhang et al., 2021). Besides the antibacterial
tissue has been demonstrated (Binnetoglu et al., 2020). Presumably, the effect of AgNPs, the authors suggested heat-induced cell proliferation
presence of an electric field should have a positive effect on the regen and wound healing. The effect of heat on the rate of wound healing has
eration of electrically conductive tissues. This hypothesis has been been repeatedly described (Du et al., 2022; A. A. Khan et al., 2004).
confirmed in vitro by Chen et al. They used PC12 neuroblastic cells Because any conductor generates heat (Joule heating), almost any CBC-
grown on BC/PEDOT/GO (C. Chen et al., 2016a). The authors demon based composite could be used to stimulate the wound-healing process.
strated prominent directed cell growth under the action of a directed
electric field, as well as the absence of cytotoxicity of the composite
10
5.3. Flexible wearable sensor systems based on the BC (Ge, Zeng, Hu, Yang, et al., 2022b; Ma et al., 2022). By
replacing water with tert-butyl alcohol, BC could be dried at atmo
Much attention has now been paid to wearable flexible sensor sys spheric pressure without destroying its 3D structure. In this case, the
tems (J. Huang, Zhao, Hao, Wei, 2022b). Such devices can transmit number of nanopores increased and BC hardened. This was followed by
information about the pressure and stretch that occurs when pressed and the impregnation of BC with a solution of potassium hydroxide (KOH)
flexed, which is necessary for advanced limb prosthetics (S. Chen, Wang, and final drying. The authors suggested that the high sensitivity to
Fei, Long, Wang, Zhang, and Chen, 2022c; Su, Liu, Lei, Wang, et al., moisture (>103 at relative humidity from 36.4 to 93 %) can be attrib
2022b); provide information about human body temperature which is uted to hydrophilic functional groups of BC nanofibers and the intro
an important factor for many diseases (Jiang et al., 2022); monitor the duction of KOH into the branched BC network. A slightly different
composition of the environment (X. Jin, Li, Zhao, Li, et al., 2021b; L. approach was chosen for the simultaneous modification of BC with GO
Yang et al., 2021), to control harmful substances around a person. Such and MXene (Ti3C2Tx), which exhibited excellent moisture-driven per
sensors often consist of a matrix and a doping material, which acts as an formance with superior mechanical properties and ambient anti
active component. However, while we enjoy the benefits that electronic oxidation (Ge, Zeng, Hu, Yang, et al., 2022a). This system is inherently a
devices bring us, electronic waste (e-waste) aggravates the environ humidity sensor, but simultaneously changing its shape opens the way
mental crisis, threatening not only our health but also the sustainable for proximity switches (Fig. 5D).
development of our economy and society. Compared to degradable Flexible electromagnetic self-powered sensors based on magnetic
polymers, e.g., poly(vinyl alcohol) (PVA), poly(glycerol sebacate) (PGS), materials are promising for use as wearable devices. BC can be an
or PPy, BC composed of polysaccharides and possessing excellent excellent biodegradable scaffold for such devices; for example, when
biodegradability at low cost, brings no pollution after disposal. doped with CoFe2O4 NPs (K. Chen, Li, Du, Hu, et al., 2022b). To obtain a
Furthermore, BC manifests a 3D interconnected network structure flexible magnetic film, BC was placed in a solution of CoCl2 and FeCl3
composed of nanofibers with diameters of 10 − 100 nm with plentiful (Co2+:Fe3+ = 1:2) and heated at 60 ◦ C for 4 h. Such a flexible electro
oxygen-containing functional groups. It has phenomenal hydrophilicity magnetic film in combination with a copper coil can be used to produce
and mechanical strength due to hydrogen bonding, which endows its self-contained “smart clothes” sensors (Fig. 5E). The correlation coeffi
hydrogel with many outstanding properties including high porosity, cient between the signal amplitude and the movement speed is 0.994,
large specific surface area, low elastic modulus, and high flexibility and that between the signal frequency and the movement speed is 0.973,
which are higher or equal to natural biomaterials including plant-based which proves the autonomy of such “smart clothes” and their ability to
polysaccharides (e.g., cellulose), and animal derived polymers (e.g., track a person’s movement.
collagen and silk fibroin). All of these make BC is an ideal candidate not Hydrogel-based sensors (Lu, Hu, Li, Wang, et al., 2022b; J. Wang,
only for the role of a matrix but also as a sensor agent (J. Huang, Zhao, Dai, Wu, Ye, Yuan, and Jia, 2022c) and organogels (Guo, Yuan, Huang,
Hao, Wei, 2022a). Zhang, et al., 2022a) based on BC exhibit some unique properties. The
BC can be modified in situ during its growth. For example, CNTs piezoelectric sensor, consisting of a BC hydrogel matrix and imidazo
(Hosseini, Kokabi, Mousavi, 2018b) and GO (Hosseini, Kokabi, Mousavi, lium perchlorate (ImClO4) molecular ferroelectric has a high sensitivity
2018a) can be introduced into the culture medium. This can be achieved of 4 mV kPa-1 and a wide operating range of 0.2 to 31.25 kPa, which
by physical modifications (S. Zhang, Xu, Liu, Huang, and Jiang, 2022c), exceeds the performance of most devices based on conventional func
such as simple mixing and reduced pressure infiltration (S. Chen et al., tional biomaterials (Lu, Hu, Li, Wang, et al., 2022a). Moreover, BC
2022d), ultrasonic treatment, and chemical doping (L. Yang et al., 2021; hydrogels can be completely degraded to glucose and oligosaccharides,
Zhi et al., 2021). This can also be a process of polymerization, directed and ImClO4 can be recycled and reused in the same devices, leaving no
functionalization of the surface (oxidation and nitration), hydrothermal environmentally hazardous waste.
synthesis, carbonization, and pyrolysis. The basic principles of the One of the disadvantages of hydrogels for wearable devices is the
operation of sensor systems can be classified into piezoelectric, piezor difficulty of their preparation. To eliminate this drawback without
esistive, and capacitive. The general principle of the operation of each of compromising any other characteristics, a method was proposed for a
these are discussed in the review (J. Huang, Zhao, Hao, Wei, 2022a). rapid polymerization of nanowhiskers with BC, tannic acid (TA), poly
However, regardless of the operation principle, one of the main com acrylic acid (PAA), Fe3+, and a solution of glycerol in water (Gly/H2O)
ponents can be BC. (J. Wang et al., 2022b). The action of two catalyzing agents, TA-Fe3+
Thus, a flexible high-performance pressure sensor was developed by and Gly, significantly reduced the reaction time (to 4 s) at ambient
modifying BC with aramid nanofibers (ANFs) using silver nanowires (S. temperature. With multiple hydrogen bonds and coordination between
Chen, Wang, Fei, Long, Wang, Zhang, and Chen, 2022c). A simple vac BC-TA, PAA, and Fe3+, the hydrogels showed an excellent balance be
uum infiltration method was used to obtain the BC/ANFs. Compared to tween mechanical properties (stress 203 kPa, elongation to break 1950
untreated BC, the tensile strength increased by 60.6 % after the addition %) and self-healing abilities (91 % efficiency). Tension sensors based on
of reinforcing fibers. The BC/ANFs/Ag sensor showed excellent pressure these composites demonstrated stable properties over a wide tempera
response and stability, with no noticeable reduction in sensitivity after a ture range (− 20 to 60 ◦ C).
constantly applied pressure of 5 kPa for 100 min. Organogels with a double-polymer network exhibit high perfor
Pressure can originate not only from physical contact but also from mance parameters. The covalent crosslinking polymers poly
the impact of sound. Vacuum infiltration method was implemented to vinylpyrrolidone (PVP) and polyvinyl alcohol (PVA) were chosen as the
create a BC sensor modified with MXene (Ti3C2Tx) (Su, Liu, Lei, Wang, first level of organization, and BC and calcium chloride were used as the
et al., 2022a). Subsequent assembly of the device was performed using second level (Guo, Yuan, Huang, Zhang, et al., 2022b). Thus, they
plain paper as a flexible substrate. BC/MXene composite demonstrated retained long-term stability (>15 days) in air, and the dynamic combi
excellent performance: high sensitivity in the low-pressure range nation of BC-Ca2+ and hydrogen bonds in the binary system also gives
(0–0.82 kPa:51.14 kPa-1), wide linear range (0–0.82 kPa, 0.82–10.92 organohydrogels excellent tensile strength (1.0 MPa), tensile deforma
kPa), fast sensor response/recovery time (99/93 ms), high stability tion (1300 %), and impact strength (6.2 MJ/m3) and electrical con
(5000 cycles), and the ability to capture traditional human movements, ductivity (0.034 S/cm) and self-healing ability (up to 632 % in tension).
including tapping, finger tapping, exhaling, nodding, swallowing, and The described hydrogels and hybrid organogels are promising for use in
coughing. flexible electronic skin, motion control, and soft robotics.
Measuring humidity using wearable devices is an important task. One of the important factors in wearable devices is their weight and
This challenge requires some flexible, light, biocompatible, and at the surface area. Aerogels are absolute champions in terms of their mass-to-
same time, sensitive materials. Such sensory systems can be designed surface area ratio. BC-based carbon aerogels are widely used in wearable
11
sensors because of their unique properties such as ultra-low density, possesses.

high electrical conductivity, super elasticity, and fatigue resistance
(Guo, Yuan, Huang, Zhang, et al., 2022b; X. Jin, Li, Zhao, Li, et al., 5.4. Flexible energy sources
2021a; L. Yang et al., 2021; Zhi et al., 2021). However, maintaining
good mechanical characteristics and high sensitivity remains a chal Most of the sensory systems described above require some flexible
lenge. To overcome these shortcomings, a BC hydrogel with (NH4)2SO4 energy sources. Supercapacitors and batteries can be developed using
was obtained and freeze-dried. Ammonium sulfate acts as a damping BC. We focus here on the phenomenon of electrical conductivity of
agent, preventing shrinkage and deformation of the BC structure. After modified BC, thus, separators and gel polymer electrolytes are outside
carbonization, the resulting aerogel exhibited a distributed honeycomb the scope of our consideration, because in their case the main charac
structure. The carbon nanofiber aerogels possessed some exceptional teristics of the materials are ionic conductivity and the presence of
mechanical characteristics: high compressibility (up to 99 % deforma pores. The general aspects of using BC in flexible electronics are dis
tion), superelasticity (~97.4 %, 500 cycles at 90 % compression), and cussed in the review (Lei et al., 2020). The use of BC as a polymer
stability (up to 103 cycles). Besides, the sensor has a high sensitivity electrolyte is discussed in the following review (L. Zhang, Gao, Jin, Liu,
(5.66 kPa-1) over a wide pressure range (0–28 kPa) and a short response Wu, Wu, Yang, Wang, and Wang, 2022a). In this section, we focus on the
time (~100 ms), which allows it to control the signals of the human BC as an electrically conductive component in flexible electronics.
body and physical contacts, as well as to provide voice recognition. For wearable and flexible electronics, it is necessary to create bat
Ammonia is an important pollutant that must be controlled. The teries that are appropriate in terms of their parameters. One option is a
modified aerogels based on BC demonstrated high sensitivity and supercapacitor. PAni (H. Wang et al., 2012), PPy (Y. Sun, Yang, Fan,
reproducibility for ammonia detection (X. Jin, Li, Zhao, Li, et al., 2021a; Zheng, et al., 2022a; J. Xu et al., 2013), GO (F. Guan et al., 2019), and
L. Yang et al., 2021; Zhi et al., 2021). Yang et al. modified BC with PAni, PEDOT:PSS (K. K. Liu et al., 2018) were used with BC for this purpose.
sulfosalicylic acid (SSA), and poly(2-acrylamido-2-methyl-1- One of the main characteristics of supercapacitors is their capacitance.
propanesulfonic acid) (PAMPS) (L. Yang et al., 2021). After drying, a Guan et al. achieved a capacity of 65.9 F/g at 0.4 A/g using BC/GO
sensor was obtained with a high response (21.3 for 50 ppm ammonia), structure (F. Guan et al., 2019). The authors attributed this to a large
fast response and recovery times (4.1 s and 16 s), high selectivity, and number of pores in GO, an ordered BC structure, and its high hydro
the limit of detection (LOD) of 10 ppb at room temperature. philicity. Liu et al. obtained much higher values (445 F/g at 2 A/g) due
A similar approach was used to obtain a pressure-sensitive sensor to the addition of SnO2 NPs to the structure (K. K. Liu et al., 2018). The
that can also detect the presence of ammonia (Zhi et al., 2021). This combination of GO and PAni enables fabricating a supercapacitor with a
binary opportunity became possible when BC was doped with PAni and capacity of 645 F/g at a current density of 1 A/g (Luo, Dong, Zhang, Li,
Ti3C2Tx. The resulting material can be regarded as electronic skin, which Guo, Zuo, Ye, Wang, Yang, and Wan, 2018b).
can be connected via Bluetooth to transmit data to the user’s smart The uniform deposition of the conductive polymer layer may be
phone by just touching the latter. The ammonia sensitivity of the sensor challenging. A simple and effective approach was proposed for a uni
results from the unique three-dimensional structure of the aerogel and form deposition of anion-doped PPy on the surface of positively charged
the numerous functional groups (such as –O, -OH, and –F) in MXene, BC modified with SnCl2 (Y. Sun, Yang, Fan, Zheng, et al., 2022b). PPy
which provide efficient electron transfer during sensing, and create was applied to a BC/SnCl2 membrane via in situ oxidative polymeriza
active sites for adsorption. The sensor showed a linear concentration- tion. The resulting composite electrode showed a high surface capaci
response curve at 2.5–12.5 ppm (R2 = 0.997), and the response to tance (5718 mF/cm2 at a current density of 0.5 mA/cm2) and high
these other analytes was <3 %, which is much lower than for NH3 cycling stability (86.8 % capacity retention after 10,000 cycles at 10
(56.63 % for 7.5 ppm), demonstrating excellent selectivity. Jin et al. mA/cm2).
proposed a similar system based on a BC bio aerogel modified with There are many more examples of supercapacitors based on BC,
Ti3C2Tx, but without using PAni; gold electrodes were used instead (X. which is a fairly common material for these purposes. Its mechanical
Jin, Li, Zhao, Li, et al., 2021a). The idea was to create a multifunctional stability, large surface area, and high absorption capacity are the main
pressure sensor to determine the eventual occlusion of the teeth, voice, properties that make it widely used in this application. More details on
and pulse, as well as to control exhaled ammonia, which is responsible the possibilities for creating energy storage systems can be found in a
for various endocrine pathologies. Given the eventual mass application recent review (Lokhande et al., 2022).
of this sensor in orthodontics, an ecological approach has been proposed High-temperature treatment (carbonization and pyrolysis) does not
for complete decomposition using a solution of H2O2, which meets the always cause a complete loss of flexibility in a BC-based material. Thus,
growing requirements of sustainable development. when BC is modified with molybdenum sulfide (MoS2) NPs, an anode
Thus, the detection of chemical and biological molecules is essential. material is obtained for LIB, in which no binder is required (F. Zhang
One possible solution is to use surface-enhanced Raman scattering et al., 2016). Because of the 3D framework, the material remains flex
sensors, including those based on cellulose (Ogundare & van Zyl, 2019). ible. A high specific capacity of 935 mAh/g was achieved at a current of
Typically, such systems have some disadvantages including low-cost 0.1 A/g. At a current of 1 A/g, the specific capacity was 581 mAh/g, and
efficiency, complexity of manufacturing, and poorly reproducible the long-term stability was up to 1000 cycles. A similar approach was
signal. Thus, magnetron sputtering of Ag NPs onto vacuum-filtered used in (Y. Huang et al., 2016), but the modification was performed
bacterial nanocellulose has been proposed (S. Zhang, Xu, Liu, Huang, using Fe2O3. It has been shown that an amorphous coating makes it
and Jiang, 2022c). Owing to the large specific surface area, excellent possible to more than double the capacitance compared to a crystalline
permeability, and adsorption properties of hydrophilic nanocellulose, coating. A similar strategy was used in (Wan et al., 2015); however, after
the detected molecules were uniformly distributed over the surface of carbonization, a flexible composite material BC/Fe3O4 was obtained,
the nanocellulose membrane. As a result, the sensor exhibited a high with a high reversible specific capacity of 754 mAh/g (after 100 cycles
sensitivity of 10-9 M to crystal violet, signal uniformity, and high storage at 0.1 A/g). The branched structure of pyrolyzed BC serves as a frame
stability. Ultra-sensitive pesticide detection has also demonstrated an work for the anode material for LIB based on amorphous red phosphorus
LOD of 7.8 × 10-8 M for lambda-cyhalothrin on uneven fruit surfaces. (H. Yang et al., 2018). This material, while maintaining its flexibility,
This indicates the potential for the development of SERS devices based demonstrated a high resulting specific capacity (1039.7 mAh/g after
on a branched BC structure. 100 cycles at 0.1C, 1C = 2.6 A/g) and a good stability at a high current
Overall, BC is widely used in a wide range of applications for density (retention 82.84 % after 1000 cycles at 2C).
detecting physical phenomena and chemicals. This is only possible Zhou et al. assembled a prototype of a fully flexible BC battery
because of a unique combination of properties this versatile material (Fig. 5F) (Zhou, Liu, Du, Ren, et al., 2019b). The BC surface was
12
modified during oxidation with (2,2,6,6-tetramethylpiperidin-1-yl)oxyl resulted in a significant increase in BC conductivity (Gutierrez et al.,
(TEMPO). To form an anode with high capacity, SiO2 NPs were 2012a, b). This phenomenon requires a more detailed study.
embedded to the surface and into the volume of the modified BC. It is Another problem with the practical use of BC (and CBC) is the
important to note that BC was also used as a cathode and separator. The impossibility of its drying while maintaining the ability to retain liquid.
cathode material contained LiFePO4 (LFP) particles, and the separator Many articles even contain an extra clarification of “never dried” BC
was composed of SiO2. The anode and the cathode were also doped with used (S. Khan, Ul-Islam, Khattak, Ullah, Park, 2015a). The main reason
conductive carbon to increase their electrical conductivity. To study the for this is the presence of many hydroxyl groups, which results in fibril
possibility of battery bending, the transparent polymer poly aggregation upon BC compression (during drying, the thickness of the
dimethylsiloxane (PDMS) was chosen to assemble the complete cell. As a BC film decreases to 1 % of the initial value (Skvortsova et al., 2019)). It
result, in the half-cell, the silicon-based anode exhibited reliable cycle has been shown that if a film of BC is dried at room temperature, it loses
stability (639.4 mAh/g after 400 cycles at 1.0 A/g). The discharge ca up to 90 % of its ability to retain water. This applies to both unmodified
pacity in the first cycle reaches 121.7 mAh/g while after 100 cycles the (Klemm et al., 2001) and modified BC (Yoon et al., 2006). Freeze-drying
discharge capacity was 73.4 mAh/g (capacity retention 60.1 %). The is a preferred method; however, its results are far from being satisfactory
authors argued that the stability of the complete element was not for the purposes. One option to overcome this drawback is to create
affected by mechanical bending. aerogels from BC (C. Li et al., 2020). In this case, BC retains its structure
BC has been used to form cathodes for magnesium-ion batteries (J. and many of its mechanical properties. Thus, if BC is not to be used
Zhu et al., 2020). To do so, it was doped with Ti3C2. A good charge immediately after fabrication, it has to be stored moistened in an
retention rate of 88 % after 100 cycles and an impressive specific ca appropriate solvent (and under sterile conditions if possible). No articles
pacity of 171 mAh/g at a current of 50 mA/g was achieved, which is 17 seem to have been registered where the properties of CBC composites
times greater than that of pure Ti3C2. during long-term storage were studied, except for some research on the
As discussed above, it is possible to create a completely flexible mechanical parameters of flexible devices during repeated bending/
electronic device, where both the sensor and the energy parts are BC- extension.
based. There do not seem to be many examples where BC was used as Most CBC composites are black because of the color of polymers or
an electrically conductive component in batteries. On the other hand, it NPs. However, even in the case of using transparent PEDOT:PSS, the
is its use as a polymer electrolyte or as a component of supercapacitors inherent white color of the BC does not make it possible to produce
that is currently emphasized. It is already possible to obtain a fully completely optically transparent hybrids. Some researchers have suc
flexible battery, where all the main parts are made using BC. Few ma ceeded in achieving partial transparency of BC composites by incorpo
terials appear to be used in this way. Unfortunately, it is currently not rating ionic conductive polymers (Jeon, Yoo, Park, Kim, Hyun, 2014a).
possible to conduct an ample comparison of BC-based batteries with Jeon et al. also showed that agitation increases the fibril diameter,
conventional ones due to scarce information. We can only state that all which makes cellulose less transparent. On average, the transparency of
useful properties and approaches to synthesis and modification the samples was approximately 75 % at a wavelength of 550 nm (Jeon,
described for the sensors are applicable for flexible batteries. Yoo, Park, Kim, Hyun, 2014b). Jung et al. achieved a transparency of
70.3 % and a conductivity of 5.3 × 10-3 S/cm using MWCNTs (Jung,
6. Some issues of CBC applications Kim, Kim, Kwon, et al., 2008b). A transparency of 50 % in the 800 nm
region was achieved by introducing vanadium oxide NPs into the BC
Despite a large number of examples of CBC composites, none has structure (Gutierrez et al., 2012a). Nanocomposites with Ag nanowires
reached mass practical application. Among the common issues of new also exhibit a transparency of approximately 80 % (Lv, Zhou, Zhao, Li,
technologies there is the need to optimize synthesis methods. This Lu, Wang, Huang, Cai, Lucia, and Wei, 2018b). However, very few
concerns, among other things, the scaling of BC production methods (Ul- studies indicate the thickness of the BC film for which transparency was
Islam et al., 2020). The “valley of death” problem also affects CBC studied, which makes it difficult to compare the results.
(Siegmund et al., 2021). However, we would like to focus on some less Additional difficulties include maintaining a balance between the
obvious issues specific for CBC. mechanical characteristics of CBC (Young’s modulus, tensile strength)
One problem is the insufficient investigation of the internal structure and its conductivity. In most methods that use polymers, one or more
of the CBC after modification. No conductivity measurements have been oxidation procedures are used. It has been repeatedly shown that this
reported either for different CBC parts (surface area/inner volume). impact on BC results in a decrease in its strength (Favi et al., 2016; Hu
They are required to ensure that the physico-chemical parameters of et al., 2011; Lin et al., 2013). However, we tend to mention the work of
CBC have remained the same throughout the thickness of the composite. Cui et al., who showed the opposite effect (Cui et al., 2014). In their
Homogeneity is important when creating artificial tissues that have to be study, controlled oxidation of BC with NO2 in HNO3 resulted in an
uniform throughout the entire sample volume. In many cases, where the increased crystallinity and improved mechanical properties of BC. Based
uniformity of the conductive polymer distribution can be estimated from on this, we can assume that in each specific combination of oxidizing
transmission electron microscopy, only SEM is performed, which does agent/polymer/dopant, it is necessary to conduct a separate study to
not provide enough data on the internal structure. Modification by select the relevant time and strength of the oxidizing agent for the
conductive polymers in bulk films is most likely to occur unevenly. The required mechanical properties.
internal structure of BC may also be altered unevenly. This can lead to an Moreover, the stability of BC as a sensor material remains ques
odd conductivity distribution in CBC films, different rates of biodegra tionable. More complex studies that would reveal the features of the BC-
dation, and other unforeseen consequences. based sensor operation at different temperatures and humidity do not
Another issue worth paying attention to is the large difference in the appear to have been conducted yet. For advanced batteries, BC is
conductivities of composites obtained via similar methods. For instance, promising as a hydrogel or organogel for polymer electrolytes or as a
for PEDOT, the values of 278 S/cm (Kwon et al., 2021) or 7.3 × 10-2 S/ branched substrate for separators. Currently, BC is not widely used as an
cm (S. Khan, Ul-Islam, Ullah, Kim, and Park, 2015c) were obtained, electrode material. Apparently, this is due to incomplete research, and
representing a three-order difference. Similar examples were also the full potential of BC has not been used. We are convinced that, when
observed for other polymers (Table 1). To some extent, this can be working with such a material, the moment of modification must be
explained by some minor differences in the synthesis methods. However, combined with the process of BC growth to minimize post-doping. This
we assume that this may also be due to different measurement protocols, presents some difficulties; bacterial cultures can be affected by modifi
as the measurement of polymers conductivity is not a trivial task. In cation, and the quality of BC can decrease, and the properties degrade.
addition, in some studies, nonconductive dopants such as metal oxides One interesting direction can be the methods of post-modification with
13
sulfur, fluorine, phosphorus, and nitrogen. This would provide BC with attributed this to the high conductivity of the composite (156 S/cm), as
some new and unique properties. Besides, BC remains inaccessible to well as a unique cross-layer structure, due to which electromagnetic
many scientists because it requires microbiological laboratory de waves, even passing through one layer, are reflected from another.
partments and staff. When BC synthesis becomes a simple and accessible There are also some other similar approaches (Marins et al., 2014; Wan
process, we expect to see an explosive growth in publications, as was the et al., 2021).
case with GO, and which has not been registered to the same extent for To bolster the use of CBC in tissue engineering, it seems logical to
MXenes. create an artificial myocardium. In the myocardium, conductivity varies
greatly depending on the direction of measurement because car
7. Prospects of CBC application diomyocytes grow in certain directions (Johnston & Johnston, 2020).
However, conductivity values are within the range of 10-3 S/cm (M. Sun
In this section, we suggest some ideas that have not been imple et al., 2021), which corresponds to the conductivity of most CBC com
mented but partially discussed in published papers, and may serve as the posites. The question is how to provide “directed” conductivity? To
basis for improving some technologies. achieve this, the CBC must have an ordered structure in which the
BC modification with NPs provides a wide range of opportunities for conductivity differs depending on the direction of measurement. As for
adjusting CBC properties since NP properties can be accurately the choice of conductive dopant, in our opinion, PEDOT deserves the
controlled. For example, various methods for the synthesis of Au NPs most attention as a polymer used to create CBC for medical applications.
have made it possible to set the plasmon resonance wavelength with an As mentioned in the relevant sections, it has the best biocompatibility,
accuracy of 0.5 nm (N. G. Khlebtsov et al., 2022). This may provide mediates cell proliferation, and has already been successfully tested in
photosensitive scaffolds with multiple substance release. A similar several preclinical trials. It also had a wide range of conductivity set
approach was demonstrated by Zhang et al. through the in situ synthesis tings. This may promote using PEDOT as a conductive polymer for
of AuNPs with different morphologies on BC fibrils (T. Zhang et al., biologically relevant applications.
2010). NPs such as ZnO are known to have antimicrobial properties Powering-implanted medical devices (IMDs) remain a challenge, as
(Sirelkhatim et al., 2015). They can be used to reduce bacterial biological systems require biocompatible, stable, and miniaturized
contamination of implantable biosensors or electrodes. A similar effect power sources. Using a salinity gradient is an attractive and efficient
was observed for the BC/TiO2 (S. Khan, Ul-Islam, Khattak, Ullah, Park, way of generating electricity. Wang et al. demonstrated the operation of
2015b) and BC/Ag (Wu et al., 2018; L. Zhang et al., 2021). Besides, it is an osmotic nanoenergy generator based on a negatively charged BC/
the in situ synthesis of NPs within the BC structure that is of interest. It is MXene (B. Wang, Li, Wu, Sheng, Zhang, Han, Jin, Li, Lv, Ou, Wang, and
also possible to incorporate NPs within BC via layer-by-layer synthesis, Chen, 2022a). This nanofluidic membrane imitates an ion channel. By
as shown above. Theoretically, any NPs that are stable in the culture combining 1D nanofibers and 2D MXene sheets to provide space charge
medium, have sufficient hydrophilicity, and are not toxic to bacteria can and increase ion flux, a power density of 2.58 W/m2 was achieved with a
be incorporated into the BC structure. In addition, many conductive 100× solid electrolyte concentration gradient. Moreover, the results of
polymers allow embedding various metals (Ćirić-Marjanovic, 2013). the in vitro and in vivo evaluations demonstrated good biocompatibility
This approach makes it possible to produce composites with metals that of the hybrid membranes. The highly efficient osmotic energy conver
have not yet been used to obtain CBC. sion and good biocompatibility of the BC/MXene membrane make it a
The ability to grow BC of almost any size (matching the size of the promising tissue-embedded battery material for powering IMDs.
cultivation flask) makes it possible to provide paper-like specimens, Low-grade heat or secondary heat is found everywhere, including
close to flat. If complex 3D structures are to be created, it is necessary to sunlight, industrial processes, and the human body (He et al., 2022).
obtain gels or inks for 3D printing from BC. Several strategies can be Using this heat is a significant advantage for sustainable energy devel
used for wider CBC application by creating complex spatial structures. opment. However, much of it is wasted owing to a lack of recovery
For example, Vadanan and Lim proposed disintegration of BC using a technologies. Hydrogel thermoelectrochemical cells (TECs) represent a
cell homogenizer (Vadanan & Lim, 2022). Further introduction of simple, efficient, and cost-effective technology for collecting low-grade
PEDOT:PSS into the BC gel provided a biocompatible cast material with heat from the environment. Thus, TECs based on BC with Fe (CN)3-/4- 6
a conductivity of 0.7 S/cm. and Fe2+/3+ redox couples have been proposed. n, p-type BC-hydrogel
BC conductivity is usually related to electronic conductivity. How electrolytes were obtained using a simple impregnation method (Zong
ever, cellulose, owing to a large number of hydroxyl groups, exhibits et al., 2022). The Seebeck coefficients of n-type and p-type TECs can be
proton conductivity as well (Selyanchyn et al., 2020). The modification as high as 4.5 mV⋅K-1 for n-type TECs and 0.72 mV⋅K-1 for p-type TECs. A
of cellulose to increase its proton conductivity may include acetylation, thermoelectric proof-of-concept device connected in series with 3 pairs
sulfation, phosphorylation, and carboxymethylation. Yue et al. were of units can generate a voltage of 0.82 V and a peak power of 4.5 μW. BC-
able to increase BC proton conductivity to 3 × 10-4 S/cm due to car based TECs have potential applications in wearable electronic devices,
boxymethylation and the addition of PAni (Yue et al., 2016). Gadim energy storage and temperature measurement devices.
et al. used PSS and PEGDA as a crosslinker (Gadim et al., 2014). The To survive extreme weather, antifreeze beetles (Upis ceramboides,
conductivity value was 0.1 S/cm, which is comparable with membranes Microdera punctipennis dzungarica, and Belgica antarctica) have a smart
from Nafion (Yadav & Fedkiw, 2012). On the other hand, the BC thermal regulation system that absorbs sunlight from the black surface
membranes exhibited humidity-dependent behavior. of their body and stores energy using antifreeze proteins. To mimic this
When creating various biointerfaces, little thought is likely to be system Ji et al. developed a composite film by impregnating an organic
given to the fact that they can not only be extremely susceptible to phase change material (PCM) into a surface-modified aerogel BC/MXene
external interference but can also be deliberately hacked. In conven (Ji et al., 2022). The surface of the aerogel was hydrophobized via
tional devices, some of the challenges can be met by shielding them with silanization using CVD. This increased the capacity of heat storage by
special materials. However, when discussing flexible electronics or im 47.6 % compared to that of the unmodified BC/MXene. By combining
plants, completely different approaches and materials are required. the thermal insulation and thermal energy storage properties, submil
Interestingly, BC/CNTs can act as an EMI shield, as demonstrated by Yin limeter films with aerogel layers can maintain a comfortable tempera
et al. (Yin et al., 2022). An important property of BC is the presence of an ture range of 20–26 ◦ C for >800 s, which is more than twice as long as a
internal structure that prevents CNTs from aggregating and maintains system without films. These results confirm the possibility of a bio
their uniform volume distribution. Wan et al. recently reported a inspired combination of photothermal conversion and heat storage.
shielding composite with an efficiency of 29,141 dB cm2/g (Wan et al., Thus, biocompatibility, a fibrillar structure, the possibility of modi
2021). In that case, the film thickness was only 4 μm. The authors fication, and future improvement of methods for obtaining BC and CBC
14
will certainly lead to producing BC-based smart devices. As a material at Acknowledgements

the intersection of bioengineering and materials science, BC can become
an indispensable part of IoT devices, sensors, bioimplants, super The work was supported by the national project “Science and Uni
capacitors, and batteries, as well as other applications in the field of versities”, project No. FSER-2022-0008. Vitaly Nikolaev is grateful for
energy production and storage, acting as both an active material and an the support provided by ITMO’s Fellowship Program.
auxiliary part.
References
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Carbohydrate Polymers 313 (2023) 120850

Contents lists available at ScienceDirect

Conductive bacterial cellulose: From drug delivery to flexible electronics

1. Introduction by external stimuli. Such devices have to be based on a certain material,

Biosynthesis implies direct production of CBC during the bacteria

Fig. 3. Chemical structure of the main compounds used to create CBC.

sensors because of their unique properties such as ultra-low density, possesses.

will certainly lead to producing BC-based smart devices. As a material at Acknowledgements

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