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A Highly Stretchable, Real-Time Self-Healable Hydrogel
Adhesive Matrix for Tissue Patches and Flexible Electronics
Jun Luo, Jiaojiao Yang, Xiaoran Zheng, Xiang Ke, Yantao Chen, Hong Tan,
and Jianshu Li*
natural and synthetic components, has
been developed to accommodate various
requirements.[2] Ideal bioadhesives should
incorporate good biocompatibility, high
efficacy in a humid and/or underwater
environment, stable mechanical strength,
while also being easy to use and store.[3]
In this context, current bioadhesives have
partially reached their potential; however,
simultaneous implementation of all of the
functions mentioned above is still a significant challenge.[4] Additionally, current
clinical applications of bioadhesives assert
more claims. For instance, achieving
adhesion to areas with large deformations,
such as skin, the bladder, heart, and penis,
is particularly challenging for bioadhesives because the ductility of these organs
changes the adhesion area.[3d] Moreover,
soft and stretchable electronic adhesives
are also highly attractive for application
in wearable and implantable devices.[4a]
Furthermore, adhesives with spontaneous
self-healing capability have attracted significant attention because many materials are easily damaged in daily life, i.e.,
without external stimuli.[5] Therefore, the interest in bioadhesives is growing, and the possibilities encourage researchers to
seek novel materials that aim to meet the standards for nextgeneration bioadhesives.
Bombyx mori silk fibroin (SF), i.e., a natural protein fiber,
exhibits significant potential for biomedical applications
because of its impressive biocompatibility and tunable biodegradability.[6] Many forms of SF-based biomaterials, including
electrospinning nanofibers, sponges, and hydrogels, have been
developed by using an SF solution and exploiting the transition of the SF chain conformation from amorphous states to
intermolecular β-sheets within a period of hours to months.[6b,7]
However, the formed hydrophobic β-sheets may yield SF materials without adhesive ability and/or stretchability.[6a,8] An alternative method is the inhibition of the formation of β-sheets in
the SF, which can produce materials with flexibility and stretchability,[9] e.g., a calcium-modified plasticizing SF substrate
with high stretchability (>400%) was fabricated by the addition of calcium chloride and ambient hydration, and has been
further investigated to develop a highly stretchable (>100%)
electrode.[9a] Additionally, developing SF-based adhesives
that are, e.g., convenient for synthesis, injection, and safety,
The development of biocompatible self-healable hydrogel adhesives
for skin or wet, stretchable surfaces in air or under water is highly
desirable for various biomedical applications ranging from skin patches
to bioelectronics. However, it has been proven to be very challenging
because most existing hydrogel adhesives are cytotoxic, or poorly adhere
to dynamic or stretchable surfaces in wet environments. In this study,
multifunctional hydrogel adhesives derived from silk fibroin (SF) and
tannic acid (TA) are effectively constructed with high extensibility (i.e., up
to 32 000%), real-time self-healing capability, underwater adhesivity, watersealing ability, biocompatibility, and antibiotic properties. According to allatom molecular dynamics simulation studies, the properties of the hydrogel
adhesives, especially high extensibility, are mainly attributed to the hydrogen
bonds between TA and the SF chains in water, and water and TA molecules
can result in loose assemblies with fewer β-sheets, and more random coils
in the SF. Conductivity can also be easily introduced to the adhesive matrix
and adjusted when the strain of the adhesives occurs. Considering that it has
multiple functions and can be efficiently prepared, the proposed hydrogel
adhesives have the potential for future medical applications, such as tissue
adhesives and integrated bioelectronics.
Bioadhesives are commonly used in clinical operations,
such as tissue adhesive, hemostatic agents, and tissue sealants.[1] A variety of available bioadhesives, i.e., those based on
Dr. J. Luo, X. Zheng, X. Ke, Prof. H. Tan, Prof. J. Li
College of Polymer Science and Engineering
State Key Laboratory of Polymer Materials Engineering
Sichuan University
Chengdu 610065, P. R. China
E-mail: jianshu_li@scu.edu.cn
Dr. J. Yang
State Key Laboratory of Oral Diseases
West China Hospital of Stomatology
Sichuan University
Chengdu 610041, P. R. China
Prof. Y. Chen
Shenzhen Key Laboratory of Functional Polymer
College of Chemistry and Environmental Engineering
Shenzhen University
Shenzhen 518060, P. R. China
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/adhm.201901423.
DOI: 10.1002/adhm.201901423
Adv. Healthcare Mater. 2020, 1901423
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which are highly desired for biomedical purposes, remains
to be a challenge.[10] Specifically, tannic acid (TA), which is a
natural polyphenol compound with rich ester bonds and polyphenol groups, intrinsically exhibits biological properties of
tissue adhesion,[11] antioxidant capability, and antibiosis.[12]
It has demonstrated the potential to be a universal binder to
induce gelation of some biomacromolecules, as the biomacromolecules tend to form complex amorphous structures owing
to the strong noncovalent interactions between TA and the
biomacromolecules.[13]
An SF- and TA-based hydrogel bioadhesive has been developed recently via a facile method with wet adhesion property
and instant hemostatic ability under both wet and dynamic
biological environments, rapid sealing of severely bleeding tissues, excellent biocompatibility and biodegradability as well
as effective antibacterial protection.[14] Here, based on the SF
hydrogel that is cross-linked by TA (hereafter referred to as FT
hydrogel adhesives) via the intermolecular interactions between
SF and TA (Figure 1a), we investigate the system with many
excellent advantages of highly extensible, real-time self-healable, water-sealing, shapeable, and antibiotic for tissue adhesives. All-atom molecular dynamics (AAMD) simulation studies
are performed to study the hydrogel adhesives, especially the
highly extensibility. Furthermore, we evaluate the potential of
the adhesive as a matrix by loading conductive materials to
obtain hybrid materials with conductive performance.
FT hydrogel adhesives were spontaneously formed by mixing
an aqueous SF solution (10 wt% in distilled water) and aqueous
TA solution (10 wt% in phosphate-buffered saline (PBS), pH
3.5) with different volume ratios (Figure S1 in the Supporting
Information). The resultant hydrogels were thoroughly washed
with deionized water and labeled as FT-6/4, FT-5/5, FT-4/6,
FT-3/7, and FT-2/8, respectively, corresponding to the SF-to-TA
ratio of the 6/4, 5/5, 4/6, 3/7, and 2/8 mixtures. The colors of
these hydrogel adhesives changed from yellow to tan as the TA
content increased (Figure 1b). The fabrication process can also
be carried out by using a twin-barreled syringe (Figure 1c).
Owing to the reversibility of a hydrogen bond (hereafter
referred to as an Hbond) between amide groups of SF and
polyphenol groups of TA, the developed chutty-like FT hydrogel
adhesives demonstrated self-healing properties (e.g., as shown
in Figure 1d, the instantaneous conjoining of cut pieces of the
FT-4/6 sample). The adhesives are soft but compact owing to
their compact structure; thus, these adhesives can be molded to
form various free-standing shapes, such as spheres, cubes, cylinders, and triangles (Figure 1e). The FT hydrogel adhesives are
waterproof and can prevent water leakage (Figure 1f). A bursting
pressure test was also performed to evaluate the water sealing
strength quantitatively. According to the results of the bursting
pressure test presented in Figure S2 in the Supporting Information, the bursting pressure of FT hydrogel adhesives increased
with increasing TA content. The adhesives can be stretched
into long fibers by subjecting them to plastic deformation. It
is notable that all groups have high extensibility (Video S1,
Supporting Information), such as Group FT-6/4 demonstrated
high extension ratio of 32 000% from 5.5 mm to around
1760 mm in length (Figure 1g); this was determined by measuring the length before and after stretching the hydrogel by
hand. This ratio is much higher than that for other previously
Adv. Healthcare Mater. 2020, 1901423
reported SF materials.[9a,15] The rearrangement and/or reconfiguration of SF structures can be facilitated by the gluing action
of the TA molecules between the SF molecules, which might be
the cause of the observed high extensibility.[11] Considering the
trade-off between the mechanical properties and extensibility, it
should be noted that when the ratio is lower than 2/8, the prepared FT hydrogel adhesives exhibit poor ductility because too
many TA molecules which cause the crosslinks between SF and
TA are excessive; conversely, when the ratio is higher than 6/4,
the prepared FT hydrogel adhesives have poor adhesive ability
because less TA corresponds to few polyphenol groups.
A cryo-scanning electron microscopy (cryo-SEM) image of
Group FT-6/4 shows a porous structure (Figure 1h), which is
typical for hydrogels.[16] In addition, a porous structure can be
observed in the SEM images of freeze-dried FT hydrogel adhesives (Figure S3, Supporting Information). The orientation of
the arrangement of silk nanofibers can also be identified in the
cryo-SEM image of Group FT-6/4 after stretching (Figure 1h
inset), indicating that the hydrogel adhesive is a complex of
silk nanofibers (Figure S4, Supporting Information) that are
dynamically cross-linked by TA via the Hbonds between the SF
amide groups and TA polyphenol groups.
Interestingly, FT hydrogel adhesives prepared with different SF-to-TA ratios had a very similar water content, i.e.,
approximately 30% (Figure S5, Supporting Information),
which is lower than that of other silk-based hydrogels,[6a] and
is the reason for the high mechanical strength of FT hydrogel
adhesives. The FT hydrogel adhesives were examined over a
frequency range of 0.1–10 Hz under isothermal conditions
(22 ± 1 °C) (Figure 1i), and both storage and loss modulus
values (>1 MPa) were found to be higher than that for most
SF-based hydrogels.[15] All hydrogel adhesives were liquefied
at a shear stain above 4%, as indicated by the following result:
storage modulus < loss modulus (Figure S6, Supporting Information). These self-healing and shear-thinning properties make
it feasible to inject the materials through a needle to perform
minimally invasive injections or catheter deliveries, as their
initial mechanical strength can be completely recovered after
injection.[17]
The molecular structure of the SF in the FT hydrogel adhesives is mainly controlled by the crosslinker, TA, and water.[13]
To better understand the mechanism responsible for the
high extensibility of SF, AAMD simulations were performed
(Figure 2). The mechanical strength of SF is mainly dictated by
the crystalline domain, whereas the stretchability is determined
by the amorphous domain.[9a,18] Therefore, we simulated the
amorphous domain to explore how water and TA molecules
influence the stretchability of SF. In this study, only two extreme
conditions, i.e., in vacuum (fully dehydrated) and in water (fully
hydrated), were simulated. Accordingly, the following four
simulations were conducted: self-assembly of silk chains I) in
vacuum, II) in water, III) in vacuum with TA, and IV) in water
with TA. In Case III, TA molecules were randomly inserted into
the initial structure of the SF, and the weight fraction of TA
was 37%, corresponding to Group FT-6/4 in our experiments.
Details of the model and simulation methods are provided in
the Supporting Information.
Our simulations show that water and/or TA molecules influenced the secondary structure of silk protein, thus enabling
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Figure 1. a) Schematic of the FT hydrogel adhesive formation. b) Color of FT hydrogel adhesives according to the SF/TA ratio. c) Preparation of FT
hydrogel adhesives by mixing an SF solution and a TA solution in a twin-barreled syringe, and efficiently ejecting from the static mixer. d) Self-healing
property of the FT hydrogel adhesive. The initial sample was cut into two pieces and then brought together again; the self-healing process instantaneously yielded a recovered adhesive (Group FT-4/6 is given as an example). e) FT hydrogel adhesive molds; they can be molded into various shapes
(Group FT-5/5 is given as an example) and support their own weight. f) Waterproof property of FT hydrogel adhesives: they can patch the balloon and
instantly seal out water to create a flexible and watertight barrier (Group FT-2/8 is given as an example). g) High extensibility of FT hydrogel adhesives:
a Group FT-6/4 sample was stretched up to 32 000%. h) Microstructure of FT hydrogel adhesives: cryo-SEM images of a Group FT-6/4 sample before
and after (insert) manual stretching. i) Rheological behavior of FT hydrogel adhesives; the modulus of Groups FT-2/8, FT-4/6, and FT-6/4 are shown
for different frequencies.
high extensibility. When silk chains assembled in vacuum (i.e.,
Case I in Figure 2a), approximately 26%, 45%, and 23% of
protein residues (Figure 2e) are in the form of β-sheets, coils,
Adv. Healthcare Mater. 2020, 1901423
and turns, respectively. As an expanded structure for proteins,
β-sheets facilitate close packing of silk chains, thus excessively
increasing the density (Figure 2f) and mechanical strength.[18]
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Figure 2. Molecular simulation of the amorphous domain of SF in four different environments, i.e., in a vacuum, in water, and with and without TA
molecules. a–d) Representative snapshots of silk assemblies. e) Percentages of each secondary structure. f) Densities of the resulting packed silk
assemblies (excluding water molecules). g) Number of Hbonds formed among the amino acid residues of silk, and those formed between silk and TA.
In contrast, other secondary structures, such as coils and
turns, possess low structural regularity, and do not result
in close packing, which thus allows more freedom to adjust
chain conformations. The latter is beneficial for high extensibility. When silk chains are assembled in an aqueous solution
(Case II in Figure 2b), approximately 21%, 52%, 20%, and 1%
of the protein residues (Figure 2e) are in the form of β-sheets,
coils, turns, and helices, respectively. The introduction of water
molecules decreases the content of stiff β-sheets, but increases
the content of random coils, thus causing the silk chains to be
loosely packed. As shown in Figure 2g, the Hbond interactions
within silk proteins were substantially weakened in water, and
approximately 40% of the Hbonds completely broke. As noted
by Chen et al.,[9a] water tends to form strong Hbonds with silk
protein molecules. The number of Hbonds between water
and silk was 1808 in this study, which is approximately seven
times that formed within the silk proteins. Therefore, Hbonds
between water and silk protein should be a crucial manner for
water to break the regular secondary structure, loosen chain
assemblies, and consequently increase the extensibility of SF.
When silk chains are mixed with TA molecules in a vacuum
(Case III in Figure 2c), the content of β-sheets (11%) was
only one-half of that for Case I, but the content of coils had
increased to 65%. As an active filler, the TA molecules possess many hydroxy groups, which consequently provided many
opportunities for forming Hbonds with silk protein molecules
(i.e., the corresponding number is 296). As a negative effect,
the number of Hbonds within silk proteins was lowered to
257. However, the total amount for the silk and TA mixture
Adv. Healthcare Mater. 2020, 1901423
remained to be significantly larger than that for Case I, indicating that TA could be a good choice for crosslinking silk proteins. In Case IV, TA and water molecules were also included
in the simulation (Figure 2d). Among the four cases, the Case
IV samples possessed the highest percentage of coils, lowest
density, lowest number of Hbonds within the silk proteins, and
therefore the highest water content. Notably, the number of
Hbonds between the TA and silk protein molecules was higher
than that within the silk proteins in Case IV. This means that
these Hbond interactions induced by TA molecules cannot be
easily inhibited by a water-based solvent.
In summary, through Hbond interaction, both water and TA
molecules were found to destroy the regular secondary structure of silk proteins, particularly the β-sheets, thus leading to
loose assemblies with a higher content of random coils. Importantly, TA molecules can crosslink protein chains, even in
water; this may be a primary reason for the high extensibility of
SF. These results are consistent with the Fourier-transformed
infrared spectroscopy and X-ray diffraction results (Figures S7
and S8, Supporting Information). The number of β-sheets in
SF was found to increase with decreasing TA content for all
groups.
The adhesive strength and extensibility of the FT hydrogel
adhesives were examined by performing lap shear measurements using a universal test machine (Figure 3a,b and Video S2,
Supporting Information).[19] Fresh porcine skin tissues were
selected as representative substrates, which were tested under
moist conditions. The maximum detachment stress of the
FT hydrogel adhesive (i.e., detachment from the tissues) was
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Figure 3. Adhesive properties of FT hydrogel adhesives. a) Photograph of FT hydrogel adhesive, demonstrating its adhesive property (Group FT-4/6 is
given as an example). b) Prepared specimen; the adhesives joined two porcine skin tissue samples fixed by using a universal test machine for lap shear
testing (mean number of measurements: 3; errors bars indicate s.d.). c) Lap shear stress results for different FT adhesives. d) Typical lap shear stress–
displacement curves for different FT adhesives. e) Repeated lap shear test results for Group FT-2/8 adhesives. f) Repeated lap shear stress results for
different adhesives (mean number of measurements: 3; errors bars indicate s.d.). g) Photographs of the fresh and re-prepared adhesives gluing two
porcine skin tissue samples (Group FT-6/4 is given as an example). Note that neither detachment nor cracking was observed in any of the FT hydrogel
adhesive and porcine skin tissue samples, even after being distorted, immersed in water, distorted in water, and flushed with water. h) Photograph of
the adhesives joining two porcine skin tissue samples after being immersed in PBS for 7 days (Group FT-3/7 is given as an example). Data were presented as mean ± standard deviation (n = 3). One-way analysis of variance (ANOVA) and post hoc Scheffe test were used to analyze the data. Welch’s
robust test of equality of means and Tamhane’s post hoc test were used when homogeneity of variance could not be confirmed (using Levene’s test).
The asterisks indicate the differences between groups are statistically significant (*p < 0.05, **p < 0.01, and ***p < 0.001).
recorded as the adhesive strength. Figure 3c indicates that the
lap shear strength gradually increased with increasing TA content. Group FT-2/8 achieved a maximum adhesive strength
of 69.4 ± 5.3 kPa, which can be attributed to the existing catechol and polyphenol groups that possess a superior interfacial
binding affinity to biological tissue.[11] Interestingly, there was
no brittle fracture observed in any of the lap shear measurements because of the high extensibility of the FT hydrogel
adhesives (Figure 3d), indicating their potential as adhesives for
tissue with large deformations. Additionally, the FT hydrogel
adhesives can be used to glue different types of materials
(Figure S9, Supporting Information). We evaluated the adhesive strength of the FT hydrogel adhesives according to ASTM
D1002 by performing lap shear measurements using metal
substrates under moist conditions. As illustrated in Figure S10
in the Supporting Information, the adhesive strength also
increased with increasing TA content, and the highest stress
(12.0 ± 0.2 kPa) was measured in Group FT-2/8.
The FT hydrogel adhesives can also be repeatedly applied to
skin tissue, as the failure behavior (Figure 3e and Figure S11,
Supporting Information) and adhesive strength (Figure 3f) did
not significantly change during two re-attachments of the lap
joints owing to the excellent self-healing property of the FT
Adv. Healthcare Mater. 2020, 1901423
hydrogel adhesives. After air drying, the adhesives were stored
for a long-term period (i.e., 3 months at room temperature,
22 ± 1 °C); they were able to recover their initial adhesive state
after being immersed in water to allow swelling (Figure S12
and Video S3, Supporting Information), indicating a simplified
method to store the adhesives. The ability of fresh and re-prepared FT-6/4 samples to adhere to tissues was further evaluated
after gluing two pieces of porcine skin tissue (Figure 3g). It is
shown that, after being distorted in air and water, flushed with
water, and stretched, the adhesives maintained their adhesive
ability. Besides, the adhesives were used to directly adhere to
porcine skin tissue in water (Video S4, Supporting Information). Furthermore, the adhesives were demonstrated to maintain a connection between pieces of glued porcine skin tissue
for at least 7 days in the presence of PBS (Figure 3h), indicating
considerable potential for in vivo biomedical applications.
Then, we examined the swelling behavior, cytotoxicity, and
antibacterial properties of the FT hydrogel adhesives in vitro.
The swelling behavior of the adhesive hydrogels was tracked
over 7 days in PBS (pH 7.2). The mass swelling ratio of the
hydrogel adhesives from all groups exhibited a slight decrease
in 12 h mainly because some TA released to the surrounding
environment. After that, the mass increased with time and
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Figure 4. Biological properties of FT bioadhesives in vitro and in vivo. a) Cell viability of hDF cultured on Group FT-2/8 and FT-6/4 samples coated on
titanium plates (mean number of measurements: 3; errors bars indicate s.d.). Group FT-2/8 and FT-6/4 samples were challenged with b) 105 CFU mL−1
E. coli or c) S. aureus, for 24 h (mean number of measurements: 3; errors bars indicate s.d.). Digital images of d,e) wound treatments and f,g) wounds
7 days post-operation. Corresponding h,i) Masson staining and j,k) hematoxylin-eosin staining of healed skin; magnification: 40×. Data were presented
as mean ± standard deviation (n = 3). One-way ANOVA and post hoc Scheffe test were used to analyze the data. Welch’s robust test of equality of
means and Tamhane’s post hoc test were used when homogeneity of variance could not be confirmed (using Levene’s test). The asterisks indicate the
differences between groups are statistically significant (*p < 0.05, **p < 0.01, and ***p < 0.001).
became stable after 4 days except for group FT-2/8 (Figure S13,
Supporting Information). It might be due to Group FT-2/8
with the highest TA content in all groups released more TA
and caused more crosslinking points lost and a loosen structure to absorb more water. FT-2/8 and FT-6/4 have the highest
and the lowest TA content, respectively. The two representative
groups were selected for further cytotoxicity and antibacterial
property investigation. As shown in Figure 4a, the numbers of
dermal fibroblasts cells in Groups FT-2/8 and FT-6/4 over the
Adv. Healthcare Mater. 2020, 1901423
24 h incubation time was not significantly different from that
in the control group. The cytocompatibility of Groups FT-2/8
and FT-6/4 indicates the potential for further animal study.
Figure 4b,c shows the results of the assay for Gram-negative
and -positive bacteria models, i.e., Escherichia coli (E. coli) and
Staphylococcus aureus (S. aureus), with 105 CFU mL−1, respectively. After 24 h of incubation, the Groups FT-2/8 and FT-6/4
numbers for E. coli and S. aureus with different ratios of adhesive to bacterial suspension were significantly lower than those
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for the blank controls because of the existence of antibacterial
TA in the adhesives.[12] The highest adhesive-to-bacterial suspension ratio (200 mg mL−1) in Group FT-2/8 was found to correspond to the most potent antibacterial ability to E. coli and
S. aureus; this might be attributed to the sample having the
highest TA concentration. The FT hydrogel adhesives are rich
in TA, especially the groups with higher TA content. TA would
be released from the adhesives into the surrounding environment during the antibacterial test continually. The concentration of TA in the surrounding environment increases when
close to the adhesives. The high TA content makes the adhesives a poor substrate for bacteria survival. It is possible that
some bacteria were absorbed in the adhesives; thus they were
less in the liquid suspension to be detected. It might be the
reason that not all the groups show obvious better antibiosis
ability with increasing TA content.
Based on the assessment of adhesion and biological ability,
Group FT-2/8 with the highest TA content was chosen as the
experimental group for animal wound healing. Nontreatment
was selected as the control group. The in vivo adherence property of Group FT-2/8 was assessed by implementing the olivary
skin incision model in mice.[4a] The healing effects observed
in the nontreatment group (Figure 4d) and adhesive group
(Figure 4e) were separately examined. 7 days after the skin surgery, no inflammation was found in the tissue sample of either
group because of the adaption to mice (Figure 4h,i). However,
the worse healing effects (Figure 4f) and more disordered structures, according to the histological evaluations of the healed
skin (Figure 4j), were observed in the nonoperation group
because skin defect repair was only facilitated by the migration
of cells from the surrounding tissue. In the adhesive group, the
adhesive (Figure 4g) nearly completely sealed the wound, and
most of the aligned structures were retained in the histological
evaluations of the healed skin (Figure 4k), especially the generated epidermis, which was similar to normal tissue.[4a,20] Since
TA has been known to have the antibacterial ability and accelerate blood clotting, which are beneficial to wound healing.[12,21]
The better healing might be due to both the covering of the
wound and also the existence of TA in the adhesives. These
results demonstrate the potential of FT hydrogel adhesives in
noninvasive tissue reconstruction.
The fabrication of an adhesive conductor with the combined
features of stretchability, self-healing capability, and biocompatibility is important for the development of next-generation flexible electronics that can be applied to areas with extremely large
deformation that have proven to be extremely challenging.[22]
To investigate the potential of the FT hydrogel adhesives as
matrices for use in bioelectronics applications, we introduced
the property of conductivity to the adhesives by doping them
with a type of biocompatible conductive polymer, i.e., poly(3,4ethylene dioxythiophene):poly(styrene sulfonate) (PEDOT:PSS)
(Figure 5a). The hybrid adhesive was fabricated by mixing SF
solution with calcium chloride (CaCl2), and TA + PEDOT:PSS
solution. The resulting hybrid hydrogel (i.e., the FT-PEDOT
hydrogel adhesive) is shapeable, adherent, real-time self-healable, and highly stretchable (Figure S14, Supporting Information). The real-time self-healing property of FT-PEDOT hydrogel
adhesive is beneficial to the potential application in integrated
Figure 5. Rapidly self-healing and stretchable FT-PEDOT hydrogel adhesive-based conductor. a) Schematic of the FT-PEDOT hydrogel adhesive formation. b) Circuit and image of FT-PEDOT hydrogel adhesive connected in series with a red LED: i) original adhesive sample, ii) completely separated
adhesive sample (open circuit), and iii) adhesive sample after self-healing. c) Normalized resistance–length strain curve for the FT-PEDOT hydrogel
adhesive-based sensor. d) Optical images and corresponding normalized resistance of the sensor conformally attached to a bent gloved finger.
e) Durability test results for the sensor attached to a gloved finger, and variation of the normalized resistance due to repetitive finger bending.
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bioelectronics. Since the addition of calcium can affect the structure of SF,[9a] the lap shear test was performed to the FT-PEDOT
hydrogel adhesive. The lap shear stress of FT-PEDOT hydrogel
adhesive was 26.2 ± 4.5 MPa, which was similar to the original
FT hydrogel adhesive (28.8 ± 1.7 MPa for Group FT-5/5). It
demonstrates that the FT-PEDOT hydrogel adhesive still shows
good adhesion property after the addition of calcium chloride
and PEDOT:PSS. The conductivity of the FT-PEDOT hydrogel
adhesive was (3.17 ± 0.32) × 10−2 s m−1. After the self-healing
process, the value was (3.07 ± 0.29) × 10−2 s m−1, which was
similar to its original conductivity. As shown in Figure 5b, a
red light-emitting diode (LED) was incorporated into a circuit
with the FT-PEDOT hydrogel adhesive connected in series, and
a 6 V power supplier (Figure 5b-i). The self-healing conductivity
of the FT-PEDOT hydrogel adhesive was verified by dimming
the LED, dividing the adhesives into two pieces (Figure 5b-ii),
and observed that the LED spontaneously re-activated once the
separated pieces were brought into contact (Figure 5b-iii) in the
circuit. After the two adhesive pieces were brought into contact
with each other, the circuit was alive as a result of the two pieces
of the adhesive re-forming dynamic Hbonds at the contacted
interfaces. As depicted in Figure 5c, the normalized resistance
of our FT-PEDOT hydrogel adhesive-based strain sensor steadily
increased to 485% as the length strain increased to 300%, indicating that the FT-PEDOT hydrogel adhesive has the potential
to be used in electronic devices to accommodate large dynamic
deformations. As an example, the sensor was employed to detect
the flexibility of an index finger (Figure 5d). Once the finger
was bent, the cross-section of the FT-PEDOT hydrogel adhesive layer began decreasing with increasing length, causing the
relative resistance to increase. The resistance further increased
as the bending angle increased. Furthermore, the results of
the durability test performed under the condition of repetitive
finger bending (≈200 times) (Figure 5e) indicate good reliability
of the sensor. The FT-PEDOT hydrogel adhesive, with its high
self-healing efficiency and stretchability, is very attractive as a
matrix for the bio-application of healable electronic devices that
can accommodate large dynamic deformations.[5a]
In conclusion, we prepared SF/TA-based hydrogel adhesives
with an unprecedented level of multifunctionality. The adhesives possess characteristics of high extensibility, real-time
self-healing capability, pliability, injectability, antibiosis, and
underwater tissue adhesiveness. Additionally, the adhesives can
be stored after air drying and recovered by swelling the dried
samples. The Hbonds that formed between the amide backbone of SF and the polyphenols of TA when exposed to water
are responsible for the pliability of the adhesives; furthermore,
the water and TA molecules lead to loose assemblies with fewer
β-sheets and more random SF coils, thereby resulting in excellent extensibility of the adhesives (i.e., up to 32 000%). The
adhesives can be used as a matrix to load conductive materials
and obtain hybrid materials with conductive performance. They
can also be extended by incorporating other additives to obtain
other desired functionalities. Considering that the simple onestep preparation, which only requires an aqueous SF solution
and aqueous TA solution, can be readily scaled up, the employed
materials may have the potential to accommodate large deformation objects for multifunctional bio-applications such as tissue
adhesives, soft electronics, and human/machine interfaces.
Adv. Healthcare Mater. 2020, 1901423
Supporting Information
Supporting Information is available from the Wiley Online Library or
from the author.
Acknowledgements
The authors thank Dr. Xingyu Chen and Dr. Chunmei Ding for their
valuable contributions to discussions. Financial support from the
National Natural Science Foundation of China (grant nos. 51903175,
51925304, 21534008, and 51773128), and the Fundamental Research
Funds for Central Universities, are gratefully acknowledged. The animal
study was approved by The Animal Ethics Committee of Chengdu Dossy
Experimental Animals Co., Ltd, China.
Conflict of Interest
The authors declare no conflict of interest.
Keywords
high extensibility, hydrogel adhesives, molecular dynamics simulations,
self-healing, silk fibroin
Received: October 7, 2019
Revised: December 29, 2019
Published online:
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