Advanced Materials - 2019 - Zhang - Skin‐Friendly Electronics for Acquiring Human Physiological Signatures

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Skin-Friendly Electronics for Acquiring Human

Physiological Signatures
Yujia Zhang and Tiger H. Tao*
exercise that may last for hours or even

Epidermal sensing devices offer great potential for real-time health and days.[1,6,7] Much effort has been invested
fitness monitoring via continuous characterization of the skin for vital to increase adhesion by improving/opti-
morphological, physiological, and metabolic parameters. However, peeling mizing the mechanical properties, thick-
them off can be difficult and sometimes painful especially when these skin- ness, and structural design of the device
substrate.[8,9]
mounted devices are applied on sensitive or wounded regions of skin due to
However, just like many skin adhe-
their strong adhesion. A set of biocompatible and water-decomposable “skin- sives and transdermal patches, the strong
friendly” epidermal electronic devices fabricated on flexible, stretchable, and adhesive design in many skin-mounted
degradable protein-based substrates are reported. Strong adhesion and easy devices usually results in difficult detach-
detachment are achieved concurrently through an environmentally benign, ment after their use, causing skin irrita-
tion, pain and even secondary damage to
plasticized protein platform offering engineered mechanical properties and
the wound when used, for example, as a
water-triggered, on-demand decomposition lifetime (transiency). Human wound healing dressing.[10] Strategies to
experiments show that multidimensional physiological signals can be design epidermal devices with strong adhe-
measured using these innovative epidermal devices consisting of electro- sion and easy (preferably triggered, on-
and biochemical sensing modules and analyzed for important physiological demand) detachment properties have yet
signatures using an artificial neural network. The advances provide unique, to be developed. Moreover, technologies
for safe disposal of epidermal electronics
versatile capabilities and broader applications for user- and environmentally
(most of which eventually end up in elec-
friendly epidermal devices. tronic wastes) have been rarely explored.
Furthermore, harsh and fluctuating condi-
tions during prolonged outdoor activities
Epidermal electronics, an emerging class of wearable elec- may affect the accuracy and reliability of those skin-mounted
tronic devices that are mounted on the human skin with con- devices.[3,4] Most designs neglect these important aspects of epi-
formal contact for direct skin-sensor interactions, are especially dermal devices, hindering them from real-world applications.
appealing for the “Internet of Things” and next-generation Here we report a set of degradable epidermal electronics
wearable medical applications.[1–5] Ideal skin-mounted devices consisting of both physical and biochemical sensors that can
should naturally comply with the epidermis with conformal monitor multidimensional physiological parameters such as
contact and adequate adhesion for human objects engaged in electrocardiograms (ECG), electrooculography (EOG), and elec-
intensive and prolonged physical activities. Most epidermal tromyography (EMG) as well as temperature, strain, humidity,
devices are attached to the skin via van der Waals forces, which and bacterial infection. Using an artificial neural network
can be inefficient for moisture, oil and hair covered skins, (ANN), important physiology signatures can be detected that
especially during strong and sometimes vigorous physical are nearly unaffected by individual differences. Moreover, while
Y. Zhang, Prof. T. H. Tao Prof. T. H. Tao

State Key Laboratory of Transducer Technology School of Physical Science and Technology
Shanghai Institute of Microsystem and Information Technology ShanghaiTech University
Chinese Academy of Sciences Shanghai 200031, China
Shanghai 200050, China Prof. T. H. Tao
E-mail: tiger@mail.sim.ac.cn Institute of Brain-Intelligence Technology
Y. Zhang, Prof. T. H. Tao Zhangjiang Laboratory
Center of Materials Science and Optoelectronics Engineering Shanghai 200031, China
University of Chinese Academy of Sciences Prof. T. H. Tao
Beijing 100049, China Shanghai Research Center for Brain Science and Brain-Inspired
Y. Zhang, Prof. T. H. Tao Intelligence
School of Graduate Study Shanghai 200031, China
University of Chinese Academy of Sciences
Beijing 100049, China
The ORCID identification number(s) for the author(s) of this article
can be found under https://doi.org/10.1002/adma.201905767.
DOI: 10.1002/adma.201905767
Adv. Mater. 2019, 31, 1905767 1905767 (1 of 10) © 2019 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
15214095, 2019, 49, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/adma.201905767 by ECOLE NATIONALE D'INGENIEURS GABES, Wiley Online Library on [24/06/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
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Figure 1. Schematic illustrations and images of the skin-friendly GEPC-based TEE for acquiring physiological states. a) Proposed framework addressing
the general strategy to achieve desired goals. b) Photograph of a wearable TEE on a subject’s forearm with a magnified view in the inset. The blue
and gray dashed-lines give the outline of the transparent GEPC substrate and electrode, respectively. c) Schematic of the TEE structure, including one
AgNWs-based electrode for electro-physiology monitoring and two R-EDG-based sensors for chemo-physiology monitoring. One R-EDG-sensor pro-
vides the reference signal to eliminate interferences from fluctuating skin temperature (Temp.), relative humidity (RH.) as well as body motions. The
other R-EDG-sensor was biomodified with anti-bacterial peptides, so called BR-EDG, to quantitatively monitor the presence of bacteria on the skin. The
TEE can be triggered to decompose after providing a multidimensional data set for acquiring the physiological signatures using an ANN algorithm.
d) Schematic illustrations of the water-triggered and heat-modulated transiency. e) The tensile stress–strain curves of GEPCs with different glycerol
weight ratio under 50% RH. Inset, the age-dependent strength of human skin tissue. f) Representative adhesion-force profiles of GEPC films attached
on a pigskin substrate, with strong adhesion before/during water treatment and easy detachment afterward. Upper inset, schematic of the experimental
set-up. Lower inset, demonstration of a GEPC film (3 × 3 cm2) fully supporting a 400 g mass on hairy skin without leaving a sticky remnant or causing
an inflammatory response after water-triggered detachment. g) Peeling force plotted against displacement for GEPC films before/during/after water
treatments. Inset, schematic of the experimental set-up. h) Comparison of a commercial patch, which causes severe skin damage during/after peeling,
and our triggerable detachment design, which is damage-free and eco-friendly.
many efforts have been invested on skin electronics to enhance The ultimate goals of our wearable transient epidermal
the adhesion, conformality, and reliability of devices, we focus electronic (TEE) system are described in Figure 1a, including
on developing epidermal devices with both strong adhesion simultaneous and selective screening of a panel of electro- and
and easy detachment properties that are suitable for acquiring chemo- physiological signals, disposable material composi-
multidimensional physiological signals. These skin-friendly tion, and skin-friendly attachment/detachment for daily usage,
electronics are essential in many daily physical exercise and as well as acquiring the individualized signals to facilitate the
clinically relevant scenarios for skin-sensitive people (including accurate identification of various physiological states.
infants and dermatosis patients); this enables their use on The images in Figure 1b present the example of an on-skin
sensitive, vulnerable, and even wounded skin regions without TEE, which integrates one electrode and two in situ calibrated
causing adverse effects. sensors on a highly transparent and stretchable substrate.
Specifically, the substrate was based on a genetically engineered transient process will be fully discussed later in Figure 3. After
plasticized copolymer (GEPC), a double-network protein-based extraction from water and fully dried (so called “the after water
matrix consisting of silk fibroin as the framework, genetically treatment,” here and in other parts of the work), the GEPC
engineered resilin protein as the modifier and glycerol as the substrate intensely shrunk due to intermolecular forces and
plasticizer (Experimental Section and Figure S1, Supporting became extremely brittle (Figure 1diii). When minimal force
Information). The innovative combination of silk and resilin was applied, the TEE could now be easily detached from the
proteins retains the desirable intrinsic properties of high bio- skin and broken into degradable pieces; these aforementioned
compatibility, high flexibility, high skin adhesion, low stiffness, procedures constitute the water-triggered physically transiency
and exceptional resilience.[11–14] Silver nanowires (AgNWs) were (Figure S4, Supporting Information).
used for the skin electrodes due to their relatively low resist- The skin-friendly mechanical strength of the initial TEE was
ance compared to other conductive materials, thus providing an customized to match the age-dependent strength of human skin
outstanding signal to noise ratio (SNR).[15,16] The two sensors tissue by changing the proportion of glycerol (Figure 1e and
were based on a regenerated edge-decorated graphene (R-EDG) Experimental Section) and resilin as well as the chain length of
sheet that contained both an easily functionalized edge area silk fibroin (Figure S5, Supporting Information).[27] The resulting
and a highly conductive central area.[17,18] One sensor could GEPC gained extraordinary stability over time, hydrophilicity
be modified with the sensitive material to provide specialized and thermal stability, making it a suitable platform for skin-
chemo-physiological signals while the other unmodified one friendly TEE applications (Note S1 and Figures S5b, S6, and S7,
provides the calibration (reference) simultaneously. Here, we Supporting Information).
coated the R-EDG sheets with anti-bacterial peptides using a In addition to mechanical properties mentioned above, the
method reported previously, to obtain the biomodified R-EDG force of adhesion to the skin is another key factor that influ-
(BR-EDG), which is extremely sensitive to the presence of ences comfort; strong adhesion during usage and triggerable
bacteria (Experimental Section and Figure S2, Supporting detachment afterward are very important aspects for on-skin
Information).[19,20] Notably, the scenario outlined here is also electronics. However, currently most epidermal electronics lack
applicable to other graphene-based modification materials for an effective way to solve the conflicting demands of attachment
wearable chemical sensing.[21–23] The electrode and sensors and detachment. These processes may cause skin-damage
are embedded and consolidated in the GEPC substrate using a for millions of people (including infants) worldwide who are
multisteps mask printing and transfer technique (Experimental suffering from sensitive-skin symptoms.[7,28] Therefore, the
Section and Figure S3, Supporting Information).[24] water-triggered decomposition of TEEs is emerging as suit-
The system-level workflow of the TEE for multiplexed on- able solution. To examine the adhesion change of GEPC films
body measurements and data analysis is illustrated in Figure 1c. during water-treatment, we measured the normal (vertical)
The integration of electrode and in situ calibrated sensors allows adhesion and peeling forces of a 3 × 3 cm2 sized GEPC film
simultaneous and selective measurement of multidimensional attached to a pigskin with preload of 50 kPa via standard testing
parameters, such as ECG, EMG, and EOG as well as, tempera- method (Experimental Section and Figure S8, Supporting
ture, humidity, strain and importantly, on-skin bacterial infec- Information). Interestingly, the original moderately strong
tion via an electro-bacterial-graph (EBG); the GEPC substrate adhesion (maximum adhesion intensity around 49.36 kPa
provides a stable and conformal adhesion on human skin at initial state and 29.19 kPa after fully wet; adhesion energy
during prolonged indoor/outdoor physical activities. Moreover, around 10.77 mJ at initial state and 8.39 mJ after fully wet)
our strategy bridges the existing discipline gap between epi- was dramatically reduced to a nearly negligible state (adhesion
dermal electronics and transient electronics by merging flexible intensity 2.13 kPa; adhesion energy around 0.05 mJ) after water
electronic technologies of on-skin electrodes and sensors, with treatment (Figure 1f,g). Notably, the strong attachment between
the technologies of water-triggered and heat-modulated decom- the GEPC substrate and the skin can withstand a mass of 400 g,
posable substrates so that the epidermal electronics are dispos- even on a rough skin covered with hair. Hardly any remnants
able and eventually degradable.[1,11] In addition, we developed or irritability were observed on our volunteer’s hands after the
an ANN algorithm that acquires the physiological signatures patch had been attached for 6 h.
arising from the detected parameters while minimizing the By contrast to conventional wearable materials, such as
differences between individuals.[25,26] polydimethylsiloxane (PDMS), our GEPC film prominently
Importantly, our TEE approach demonstrates both skin- increases the adhesion force on hairy, oil, and moist covered
friendly and eco-friendly attributes by virtue of its unique mate- skin tissue (Figure S9, Supporting Information). Although
rial composition and corresponding water-triggered physical our GEPC does not reach the adhesion force achieved with
transiency. This was enabled by controlled plasticization of some commercial patches (sometimes too high for sensitive
the double-network protein-based copolymer, as illustrated in skins), it is high enough for on-skin monitoring under large
Figure 1d. In the initial state (Figure 1di), the stretchable TEE physical deformations (Experimental Section and Figures S9
can conformally attach to skin due to its skin-like mechanical and S10, Supporting Information). Besides epidermal elec-
properties and the strong adhesion between the TEE and the tronics, the strong adhesive capability of GEPC can provide
skin. Then, the water-triggered decomposition was produced adhesion to many commonly used objects suggesting broad
by rinsing the TEE with a large amount of water (Figure 1dii). applicability (Figure S11, Supporting Information). As a
During water treatment, water molecules replaced the bound proof-of-principle demonstration, we used the GEPC to fab-
glycerol without severely changing the electrical and adhe- ricate a wireless, battery-free wearable system for practical
sion properties, thus keeping the TEE operation stable. This utilizations, for instance, as the miniaturized radio frequency
identification device for bus-fare payment (Figure S12, Sup- To investigate the physical stability of epidermal electrodes,
porting Information). Additionally, the protein-based system the resistance was measured when epidermal electrodes were
demonstrates good biocompatibility and drug-loading capa- sharply and cyclically deformed. As shown in Figure 2b, the
bility indicating the potential for other applications. More sheet resistance was only marginally changed (less than 3.8%)
significantly, the unique water-triggered detachment prop- during bending to a maximum curvature of 500 m−1. After
erty will be useful for a variety of biocompatible skin devices 20 000 bending cycles at the maximum curvature, the electrode
that require facile detachment after the designated lifetime retained its resistance to within 2.6%, which is in sharp con-
without causing skin damage (Figure 1h and Figure S13, trast to the bending response of commercial sputtered indium
Supporting Information). tin oxide electrodes.[15] Additionally, the tolerance of the epi-
The feasibility to integrate flexible conductive materials on dermal electrodes to long-term storage in ambient atmosphere
the GEPC substrate greatly facilitates the fabrication of epi- is presented in Figure 2c. A resistance variation of 5.8% was
dermal electrodes. Such electrodes have excellent robustness, obtained after 7 weeks in storage. Importantly, the as-fabricated
malleability, and low resistance (impedance) that bond with the electrodes also demonstrate excellent conductive homogeneity
skin for high-fidelity electro-physiological signal recording. As (Figure 2c inset).
shown in Figure 2a, by tuning the loading quantity of AgNWs, With these advances in developing epidermal electronics,
we could modulate the performance of epidermal electrodes and many different sensing materials can be incorporated into
fabricate a robust hybrid network with extremely low resistance wearable chemo-physiological monitoring devices. The key
(impedance). For instance, when the load applied to AgNWs requirements of biocompatibility, mechanically robustness,
reaches 50 µg cm−2, the sheet resistance drops to as low as electrochemical stability, and facile functionalization make
9.66 Ω sq−1, which is superior to many recently reported flexible graphene-based sensors stand out for real-time on-skin
electrodes.[15,29] Note that conventional biocompatible conduc- analysis.[30,31] A variety of electrical techniques have proven
tive materials including gold, carbon nanotube, and graphene, successful in the laboratory using graphene materials and
can be used as epidermal electrodes with GEPC; we employed protein substrates. The majority of these studies are focused
AgNWs, considering the tradeoff between the conductivity and on mechanically enhanced materials but lack selectivity for
economical cost (Note S2, Supporting Information). specific chemicals or the capacity for in situ calibration.[32]
Figure 2. Performance characterization of the TEE. a) Sheet resistance of the epidermal electrode as a function of load applied to the AgNWs. Inset:
electrode impedance in the frequency domain. b) Normalized resistance variation when the epidermal electrodes were subjected to cyclic bending.
Insets: released (left) and bent configurations (right). c) Normalized resistance variation when the epidermal electrodes were stored at ambient
conditions. Inset: area mapping of the sheet resistance measured on an 8 × 8 point grid. d) Normalized resistance variation and corresponding gauge
factor of R-EGD sensors under an applied tensile strain. Inset: cyclic strain test. e) Normalized resistance variation of R-EGD sensors as a function
of temperature and humidity. f) Real-time responses of the normalized resistance variation of BR-EGD sensors with different E. coli concentrations
(CFU mL−1). Inset: schematic shows the binding of pathogenic bacteria by BR-EDG.
However, the selectivity and calibration for chemical sensors the Experimental Section). Furthermore, both the number and
are crucial, because in practical applications, the contamina- type of bacteria affected the resistance response, indicating that
tions and interferences from harsh and fluctuating conditions BR-EDG sensors are suitable for real-time analysis for the pres-
during prolonged outdoor activity may affect the reliability and/ ence of bacteria (Figure S19, Supporting Information).
or accuracy of on-skin detection.[4,26] To this end, we devised More significantly, other responses of BR-EDG sensors,
a new strategy to improve detection accuracy, using two sym- such as strain, humidity and temperature, were the same with
metrical sensors based on the R-EDG with improved sensitivity R-EDR sensors (Figure S20, Supporting Information). Note that
to achieve in situ calibration for on-skin bacterial monitoring our TEE approach integrates the BR-EDG sensor with R-EDR
(Note S3, Supporting Information). sensor, thus allowing a real-time implementation of calibrating
As mentioned above, the R-EDG exhibits higher in-plane the sensor readings on the basis of environmental variations.
crystallinity compared with conventional soluble graphene When our TEE device is attached to the skin, the signal readout
oxide (GO), thus resulting in higher conductivity (Figures S14 provides accurate assessment of skin hygiene, an important
and S15, Supporting Information).[17] Meanwhile, when first line of defense against pathogenic threats at the level of
loading was increased, the sheet resistance was increased skin infection.
while maintaining its conductive homogeneity (Figure S16, As stated earlier, the skin-friendly detachment and eco-
Supporting Information). This R-EDG sensor could measure friendly degradation of TEE are grounded in the water-triggered
strain, humidity, and temperature. Figure 2d shows the nor- decomposable GEPC substrate. Hence, it is necessary to experi-
malized resistance change of the R-EDG sensor as a function mentally and theoretically address the performance variations
of applied strain. The sensitivity of the sensor at different during the process of decomposition. The chemistry of the
strains, so called gauge factor, exhibited two distinct regimes. water-triggered decomposition at the molecular level is shown
The gauge factor is around 2–12 when the applied strain was Figure 3a. In principle, glycerol molecules act as the plasticizer
below 40%. At a higher strain of 40–60%, the GF increased to replace the incorporated water in protein hydration and to
from 12 to 50, that is comparable with other state-of-the-art form intensified hydrogen bonds with the peptide matrix,
carbon-based strain sensors, suggesting its application as a resulting in the initial stabilization of α-helical structures
wearable body-motion sensor (Figure S17, Supporting Informa- in the films, as opposed to random coil or β-sheet structures
tion).[33,34] This can be explained by the relative sliding of the (Figure S21, Supporting Information).[36,37] It is hypothe-
neighboring R-EDG sheets in the low strain regime and the sized that the glycerol interaction occurs predominantly with
complete separation in a high strain regime.[32,33,35] The strain serine and tyrosine residues due to their polar side chains.[38]
sensor showed great durability, since the response did not show Notably, compared with the soluble unplasticized initial hybrid
significant variation by loading–unloading tensile strain cycles copolymer, the increased crystalline domains render the GEPC
of 50% for over 5000 cycles. The results are attributed to the film water-insoluble and greatly improve the mechanical and
robust combination between GEPC and R-EDG. In addition to thermal robustness of GEPC film, while maintaining the out-
the strain and body motion, it is essential for wearable devices standing transparency and biocompatibility, so that it is capable
to be able to monitor surrounding humidity and temperature. to interface with skin tissues and dope with other biological
The normalized resistance variation of the R-EDG sensor under molecules.[38]
relative humidity from 20% to 100% and temperature from The water-triggered physical transiency is initiated by intro-
20 to 140 °C is shown in Figure 2e. The responses showed linear ducing large amount water into the GEPC matrix. During the
correlation with each environmental condition, thus indicating water treatment, glycerol molecules bound to the silk fibroin
their potential as wearable temperature/humidity sensors. chains are replaced by water molecules thereby releasing the
The most significant property of R-EDG sensors is their capa- glycerol molecules which diffuse into the surrounding solu-
bility to be functionalized with active materials to sense defined tion. Subsequently, when the surrounding water is removed,
chemical and biological species. In this context, we chose a the GEPC matrix remains reasonably stable and robust due
naturally inspired, chemically synthesized antibacterial peptide to water-mediated hydrogen bond formation, thus keeping the
as a proof-of-principle demonstration of robust biorecognition operation of GEPC-based TEE constant; the electrical as well
in TEE devices.[19] Unlike antibodies, the peptides are signifi- as adhesive properties are not altered until the substrate is
cantly more stable and exhibit broadband detection for a range fully “dry.” Notably, this stable operation period can be length-
of pathogenic bacteria.[20] Therefore, after coating with the ened by simply keeping the device wet, for instance, by sweat.
peptide, the R-EDG-derived BR-EDG sensors were capable of Eventually, the “wet” GEPC film will gradually lose the bonded
detecting bacteria on the skin with high sensitivity. water by evaporation and become fully dehydrated. This
The synthesized antibacterial peptide exhibited high purity allows the protein chains to adopt a more thermodynamically
(Figure S18, Supporting Information). Raman spectroscopic stable state in the form of enriched β-sheets (as validated by
analysis of the BR-EDG surface indicated successful peptide Fourier transform infrared spectroscopy in Figure S21, Sup-
binding (Figure S14e, Supporting Information). The interac- porting Information). Finally, the enriched β-sheets release
tion specificity of Escherichia coli (E. coli) cells with BR-EDG the inter-molecular bonding energy, resulting in shrinkage of
sensors was analyzed by electrically measuring the resist- the GEPC substrate and completing the decomposition of the
ance. As shown in Figure 2f, the existence of bacteria caused TEE device.
a conspicuous decrease in the resistance of the BR-EDG sen- To assess this transient process, we characterized the corre-
sors in a reasonably short time while for pure R-EDR sensors sponding resistance and adhesion energy change of the TEE.
(control), the resistance remained unchanged (see details in As shown in Figure 3b, the resistance of epidermal electrode
Figure 3. Water-triggered decomposition of the TEE with stable performance after fully wet and rapid degradation after fully dehydration.
a) Schematic illustrates the chemical changes during the transient process. b) Normalized resistance and corresponding normalized mass of the
GEPC-based electrode during the water-treatment and subsequent dehydration. c) Demonstration of the conductivity change of the GEPC-based
electrode (adhered on a paper) during the transient process in a circuit, in which the electrode connects a power source to a light-emitting diode.
d) Monitored EMG signals using the GEPC-based electrodes and commercial patches, both under fully wet conditions. The gray regions describe
when motions happened. e) Heat-modulated transient lifetime of the GEPC-based sensors. Left panel: resistance decrease during the dehydration
process caused by the water-triggered shrinkage, followed by rapidly increase accompanying device decomposition. Right panels, photographs
of an R-EDG-based sensor under visible and infrared light, which can function as wearable heater to modulate transient lifetime by connecting
to a 5 V power source.
first increased by a factor of about two compared to the initial TEE and skin tissue (Figure S22a, Supporting Information)
state because of the water-induced swelling after completely during the dehydration process. Notably, compared with initial
wet. Then, the resistance remained stable during the period state, the adhesion between the TEE and skin after it was com-
of dehydration. As evaporation of water within the copolymer pletely wet was still strong enough before complete dehydration
(corresponding to the mass variation) finished, the resistance (and decomposition) to provide stable on-skin monitoring. For
rapidly increased because of microsized cavities (defects) left example, the adhesion energy only decreased by around 30%
in the self-assembled protein structure (Figure S4, Supporting after the TEE was completely wet for 1 h. To demonstrate its
Information). We also evaluated the adhesion energy between robustness in the wet state, the GEPC-based electrode was
spread onto a paper as a conductor serving to connect a light- The systematic schematic is depicted in Figure 4a. The TEE
emitting diode to its power source. The constant light emission array currently consists of 3 pairs of TEEs respectively attached
indicated that the electrode could proper function in the wet to the left chest for the ECG, corner of the eye for the EOG
condition (Figure 3c). and arm for the EMG. The TEE array could simultaneously
It is worth emphasizing that there is a difference between the provide electro- and chemo- physiological signals, and here
completely wet state and partially wet state in the water-triggering we chose the BR-EDG sensors for EBG. The four types of sig-
decomposition process. For instance, under actual conditions, the nals were first gathered by a multichannel data collector and
sweat excretion from skin ranges from 0.1 to 2 µL min−1 cm−2, subsequently all collected data was sent to a computer. Next,
which is not enough for the water-triggered decomposition.[4,26] we used a specified signal processing algorithm to process
This underlines the advantage of our GEPC in preventing trig- the raw data containing signal filtering, wavelet transform for
gering decomposition in error. Specifically, during the mole- electro-physiological signals and extraction of the representative
cular replacement procedure, the amount of water required is features (Experimental Section and Table S1, Supporting Infor-
dependent on the amount of glycerol present. In other words, if mation). Totally 12 features (3 for each signal) were extracted
the amount of added water is less than a certain threshold value, and set as one input vector for the supervised ANN to classify.
then the copolymer will remain robust and stable after drying. We programed the ANN with 24 hidden layers and 4 output
This threshold value depends primarily on the glycerol content as classifications, which were labeled as vigorous, exercising, tired,
well as the film thickness. We designed the GEPC to have high and stimulated, corresponding to the physiological status from
sweat tolerance: the adhesion energy only decreased 20% after active to fatigue (see details in the Experimental Section, code
5 sweat-dry cycles, indicating that the device can be used for daily in Note S4, Supporting Information). The classification accu-
physiological monitoring (Figure S22b, Supporting Information). racy improves with the number of input data and we trained
Owing to the high conductivity and sweat tolerance of the the ANN with 160 vectors of data obtained from 10 volunteers
AgNWs based epidermal electrodes, we can use the TEE (Table S2, Supporting Information).
to detect many electro-physiological signals during intense The collected signals from TEE array are shown in
exercise. For example, using two TEEs attached on a volun- Figure 4b,c. The electro-physiological signals show a good
teer’s arm, we collected the EMG signals during weightlifting SNR by virtue of the conformal adhesion and low impedance
(Figure 3d and Figure S23, Supporting Information). Worth of TEE, even under sweat interference during exercising. On
noting, our TEEs exhibit a higher SNR compared with commer- the other hand, the in situ calibrated bacterial sensor indicated
cial EMG patches under both clean and sweat-infused states the on-skin hygienic deterioration during and after perspira-
because of the more conformal contact between TEE and the tion. The increased bacterial signature could come from either
skin and the stable performance after becoming wet. or both bacterial proliferation on the skin and sweat-induced
In addition to electrodes, the sensor component of the TEE bacterial adsorption from the surrounding air.[20,26] Such
was also evaluated upon becoming wet. The resistance variation electro- and chemo- signal integration provide a comprehensive
of the R-EDG sensors is illustrated in Figure 3e. Analogous to training database of the personal physiological states for ANN
electrode, the resistance of sensor was reasonably stable until (Figure S24, Supporting Information).
complete dehydration. Interestingly, one difference was the To estimate the classification performance of the trained
slightly decrease in normalized resistance just before decomposi- ANN, we plotted the confusion matrix in Figure 4d and
tion. This could be ascribed to matrix shrinkage, thus decreasing Figure S25, Supporting Information. The testing accuracy
the distance between different R-EDG sheets. For transient elec- reached to 96.9% for the training database, underlining the
tronics, one key aspect is the control of device lifetime via the deg- proper data collected by the TEE array and the adequacy of
radation process. In this respect, we control the heat-modulated the ANN algorithm. Motivated by this result, we used the
lifetime of TEE using the R-EDG sensor as an electrical heater, post-trained ANN to classify new inputs of a human subject’s
thus modulating the water evaporation speed and consequently daily movements (continuous 24 h). Note that the training and
the rate of device decomposition (i.e., device lifetime). new data came from a diverse group of volunteers (Table S2,
Monitoring physiological state is of the utmost importance Supporting Information). The classified physiological states
to people involved in physical work because the energy deficit varied sequentially from vigorous to tired during running
and muscle fatigue severely impair the actual performance and process, and were consistent with the subjective feeling of the
increase the risk of injury.[3] However, our brain cannot always volunteer subject. Moreover, after drinking caffeine-containing
realize body fatigue in real-time due to the screening by cer- energy beverages, the classified state changed correspondingly.
ebral activity and other complex physical/chemical causes.[26,39] These classification results demonstrate that the system which
Recently, emerging machine learning techniques have devised integrated the skin-friendly TEE array with the supporting
an appropriate method to solve this complex problem using the ANN algorithm could accurately acquire physiological states;
pattern recognition ANN algorithm.[25,40,41] Nevertheless, there such systems may facilitate fundamental physiology studies for
are currently no suitable sensing platforms and corresponding future personalized healthcare applications.
large-scale datasets to train the algorithms. For this purpose, we We have demonstrated our ability to achieve both strong
used a set of TEEs and a specified ANN algorithm as a proof-of- adhesion and easy detachment using silk proteins as transient
principle demonstration to show that the TEE array can be used substrates for biocompatible and water-decomposable epidermal
to acquire the signatures of physiological states, classify them electronics for real-time multimodal physiological moni-
into 4 typical categories and explore the variation of these states toring. Compared to other epidermal devices, our devices are
during daily movement. advantageous for daily applications for the following reasons:
Figure 4. Acquiring physiological signatures from multidimensional signals collected by TEE devices. a) Schematic illustrates the algorithm architec-
ture used for identifying physiological states from input information. ECG, EMG, and EOG are obtained by the electrodes. EBG is monitored by the
BR-EGD sensor with R-EDG-based sensor as calibration (control). The right part of the figure schematically describes the architecture of ANN and
four typical output classifications. The physiological states are vigorous (before exercise), exercising, tired (after exercise), and stimulated (ingested
stimulant, for instance caffeine). b) Typical electrophysiological signals during physical exercising monitored by a set of TEEs adhered to various skin
positions. c) Normalized resistance of the sensors and the calibrated result, demonstrating the sweat-induced bacterial signature on the skin increasing
during and after exercising. Gray region represents when subject was running. d) The test confusion matrix of post-trained pattern recognition ANN,
with optimized accuracy up to 96.9%. e) Using the post-trained ANN to classify new inputs of a human subject’s daily movements over 24 h. The
subject started running from the 1st until the 2nd hour and drinking a caffeine-contained energy beverage at the 4th hour.
1) universally strong device adhesion on dry, wet, oily, and hairy of biocompatible, conformal, adhesive, user- and environmen-
skins and water-triggered detachment without causing irrita- tally friendly epidermal devices.
tion, pain or damage to the skin during peeling; 2) good device
performance under wet conditions in terms of both adhesion
strength and sensing capabilities; 3) devices are nearly insen-
Experimental Section
sitive to environmental variations by employing a two-sensor Materials: The synthetic procedures of silk fibroin with different
and self-reference design for in situ calibration; 4) multidi- chain length, 64mer resilin protein, R-EDG and anti-bacterial peptides
mensional physiological parameters measured by electrical are reported previously.[14,17,20,27] The AgNWs were purchased from
Aladdin with length of 200 µm. To fabricate BR-EDG, the antibacterial
and biochemical sensors enabling more accurate and robust
peptide was first dissolved in DI water at a concentration of
analysis using an ANN algorithm. 1 mg mL−1. A volume of 200 µL of the peptide solution was dropped
The silk proteins employed are known for their optical onto 1 mg R-EDG, followed by incubation for 15 min and drying. To
transparency, biocompatibility, bioresorbability, mechanically fabricate GEPC, first the purified silk fibroin solution (around 10%
robustness and flexibility in addition to the benefits of relative w/v) was mixed with purified resilin solution (10 mg mL−1) with ratio
abundance and low cost. Importantly, silk proteins and thus of 1:1. Then, the double-network protein-based matrix was incubated
for 30 min at 4 °C. Next, pure glycerol was added at weight ratios of
silk-based devices can be readily functionalized via appropriate
0%, 5%, 10%, and 20%, followed by gently mixing on a commercial
doping with various molecules for different diagnostic and shaker. Finally, the blended solution was placed in 4 °C for storage.
therapeutic purposes, such as wound healing and controlled Fabrication of the TEE: First, the AgNWs, R-EDG and BR-EDG
drug release. Our advances offer a promising path for a new set were respectively dispersed in the diluted GEPC solution (one-tenth
concentration) at various loading quantity. Then the different blended further measurements. The artificial sweat was also used for cyclic
solutions were sequentially brushed on a patterned stencil mask placed measurements and comparison with commercial patch (PE-based
on a clean pre-stretched PDMS substrate (5 mL solution, substrate size electrode). The sweat contains 22 × 10−3 m urea, 5.5 × 10−3 m lactic acid,
of 100 cm2, under 10% strain), using the reported directional liquid- 3 × 10−3 m NH4+, 0.4 × 10−3 m Ca2+, 50 × 10−6 m Mg2+, 5 × 10−6 m uric
transfer technique.[42] Therefore, the loading quantity could be calculated acid, 100 × 10−6 m glucose, 8 × 10−3 m K+, and 100 × 10−3 m Na+. For
via dividing the total doping amount by substrate size. After cured at on-body exercising analysis, EMG signals were obtained while bending
60 °C for 10 min, the strain was released and GEPC solution was spin- the forearm toward the body at 90° for 2 s. All signals were collected
coated on the thin conductive layer and cured at room temperature using a multichannel data collector (USB-6003, NI).
for 3 h in a sterile fume hood, forming the TEE with thickness around Other Measurements: The FTIR spectra were obtained using the FTIR
30 µm. Finally, copper wires were attached to the pin position using spectrometer (VERTEX 70v, Bruker) from the wavenumber of 4000 to
silver paste. To attach the TEE onto human skin, only spraying a droplet 600 cm−1. Various GEPC films were cut into 1 cm2 to be tested. The
of water to the target position before attaching is needed. The initial optical properties were studied using a fiber spectrometer (FLAME-
strong adhesion force can be intensified by adding a soluble thin silk S-XR1, Ocean Optics). SEM images were obtained through Hitachi
film (≈10 µm) between TEE and skin.[43] S4800 at an acceleration voltage of 5 kV under secondary electron image
Mechanical Measurements of GEPC-Based Devices: Stress–strain (SEI) mode. The surface morphology was acquired using an atomic
curves are obtained by a CMT4204 mechanical tester (SUST, China). force microscope (AFM) system (Anasys Instruments, CA, USA), which
Tensile tests were conducted for more than three samples for each of allows high spatial resolution measurement using contact mode AFM
the conditions at a speed of 1 mm min−1. An environmental chamber detection. The static contact angles were measured using a contact
(LichenTech, China) was used to control the relative humidity. The angle meter with a CCD camera (DSA25, KRÜSS, Germany).
relative humidity could be automatically tuned by connecting an ANN Architecture and Design: The core algorithm is written in Python
ultrasonic humidifier with the chamber and the relative humidity values (3.6.4) via invoking functions from MATLAB (R2019a). In this context,
are measured by commercial humidity meter. The mechanical properties the scaled conjugate gradient backpropagation was chosen as the
of human skin tissue with different ages are reported previously.[44,45] training function considering the tradeoff between speed and accuracy.
Adhesion Measurements: Using a custom-built equipment based The number of hidden neurons was set as 24 to complete the input
on a CMT4204 mechanical tester (SUST, China), adhesive patches vector (12 features). The input training database was randomly divided
(size: 3 × 3 cm2) with different materials were attached with a preload into 3:1:1 for training, validation, and testing.
of 50 kPa to the pigskin substrate until failure occurred in the pull-off
direction.[9] The postmortem pigskins for adhesion tests were obtained
from a local market and stored frozen, as following well-established
protocols. To test the device’s adhesive performance in different Supporting Information
conditions, the normal adhesion forces were measured in dry (relative
Supporting Information is available from the Wiley Online Library or
humidity ≈50 %) and wet conditions (covered with water). Specifically,
from the author.
the preload was applied to the sample for 30 s. After removing the
preload, the negative force corresponding to the pull-off force was
obtained by detaching the samples from the pigskin substrate. For the
peel-off test, the adhesive patches were bonded to a metal string and Acknowledgements
attached to the pigskin substrate. Samples were lifted off at a constant
test velocity of 5 mm min−1 with the custom-built equipment, and force- This work was partially supported by the National Science and
displacement profiles were measured. All measurements were repeated Technology Major Project from Minister of Science and Technology,
at least 5 times at ambient temperature, with average values plotted China (Grant No. 2018AAA0103100), the National Science Fund for
throughout all figures. The compared commercial patch was purchased Excellent Young Scholars (Grant No. 61822406), the National Natural
from a local drug store using the over-the-counter patches such as Science Foundation of China (Grant No. 61574156) and Shanghai
Yunnan Baiyao and larger-scale Band-Aid. Outstanding Academic Leaders Plan (Grant No. 18XD1404700). The
On-Skin, Animal and Bacterial Experiments: All animal and human authors thank Tao Huang, Prof. Guqiao Ding (Shanghai Institute
tests are approved by the Institutional Animal Care and Use Committee of Microsystem and Information Technology, Chinese Academy of
of Fudan University (201802188F). All human involved in this context are Sciences) and Prof. Xiaoxia Xia (Shanghai Jiao Tong University) for
fully volunteered and give written, informed consent before participation assistance in preparing materials. The authors are also grateful to all the
in the study. For wound demonstration, Sprague–Dawley rats (six to volunteers for their cooperation in this study.
eight weeks old) were first anesthetized with an intraperitoneal injection
of a ketamine/xylazine mix. After that, the back skin was shaved
and cut to create wounds that were subsequently covered with TEE Conflict of Interest
and commercial patch. Then the body of rats was fixed to a custom-
built equipment to prevent the rat from ripping it off. After two days The authors declare no conflict of interest.
culturing, the commercial patch was peeled off, causing the damage of
the wound. In contrast, the TEE demonstrates negligible damage after
water-triggered detachment. For bacterial experiments, Staphylococcus Keywords
aureus (Newman) and E. coli (W3110) with different concentration were
selected to test the responses of BR-EDG sensor. The concentration epidermal electronics, machine learning, physiological monitoring,
was tested using the relative optical transmittance (Infinite M200 Pro, resilin proteins, silk protein, transient electronics
TECAN). For detection of bacterial cells, 10 µL bacterial solution was
pipetted onto the sterilized BR-EDG sensor. After 30 s incubation, Received: September 4, 2019
the sensor was placed in heat oven (60 °C) for 2 min and ambient Revised: September 27, 2019
temperature for 2 min before detection to eliminate the interferences Published online: October 17, 2019
from temperature and humidity.
Electrical Measurements: Electrical properties for TEE were measured
by a semiconductor parameter analyzer (Keithley 4200-SCS, Tektronix).
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Advanced Materials - 2019 - Zhang - Skin‐Friendly Electronics for Acquiring Human Physiological Signatures

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Skin-Friendly Electronics for Acquiring Human

exercise that may last for hours or even

Y. Zhang, Prof. T. H. Tao Prof. T. H. Tao

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