Simultaneously Optimize the Response Speed and Sensitivity of Low Dimension Conductive Polymers for Epidermal Temperature Sensing Applications

Abstract

Low dimension poly(3,4-ethylenedioxythiophene) poly (styrenesulfonate) (PEDOT: PSS) has been applied as resistor-type devices for temperature sensing applications. However, their response speed and thermal sensitivity is still not good enough for practical application. In this work, we proposed a new strategy to improve the thermal sensing performance of PEDOT: PSS by combined micro/nano confinement and materials doping. The dimension effect is carefully studied by fabricating different sized micro/nanowires through a low-cost printing approach. It was found that response speed can be regulated by adjusting the surface/volume (S/V) ratio of PEDOT: PSS. The fastest response (<3.5 s) was achieved by using nanowires with a maximum S/V ratio. Besides, by doping PEDOT: PSS nanowires with Graphene oxide (GO), its thermo-sensitivity can be maximized at specific doping ratio. The optimized nanowires-based temperature sensor was further integrated as a flexible epidermal electronic system (FEES) by connecting with wireless communication components. Benefited by its flexibility, fast and sensitive response, the FEES was demonstrated as a facile tool for different mobile healthcare applications.

Full text

ORIGINAL RESEARCH
published: 19 March 2020
doi: 10.3389/fchem.2020.00194
Frontiers in Chemistry | www.frontiersin.org 1March 2020 | Volume 8 | Article 194
Edited by:
Weiwei Wu,
Xidian University, China
Reviewed by:
Soong Ju Oh,
Korea University, South Korea
Han Jin,
Shanghai Jiao Tong University, China
*Correspondence:
Xuexin Duan
xduan@tju.edu.cn
Specialty section:
This article was submitted to
Nanoscience,
a section of the journal
Frontiers in Chemistry
Received: 27 September 2019
Accepted: 02 March 2020
Published: 19 March 2020
Citation:
Zhou C, Tang N, Zhang X, Fang Y,
Jiang Y, Zhang H and Duan X (2020)
Simultaneously Optimize the
Response Speed and Sensitivity of
Low Dimension Conductive Polymers
for Epidermal Temperature Sensing
Applications. Front. Chem. 8:194.
doi: 10.3389/fchem.2020.00194
Simultaneously Optimize the
Response Speed and Sensitivity of
Low Dimension Conductive Polymers
for Epidermal Temperature Sensing
Applications
Cheng Zhou, Ning Tang, Xiaoshuang Zhang, Ye Fang, Yang Jiang, Hainan Zhang and
Xuexin Duan*
State Key Laboratory of Precision Measuring Technology & Instruments, Tianjin University, Tianjin, China
Low dimension poly(3,4-ethylenedioxythiophene) poly (styrenesulfonate) (PEDOT: PSS)
has been applied as resistor-type devices for temperature sensing applications. However,
their response speed and thermal sensitivity is still not good enough for practical
application. In this work, we proposed a new strategy to improve the thermal
sensing performance of PEDOT: PSS by combined micro/nano confinement and
materials doping. The dimension effect is carefully studied by fabricating different sized
micro/nanowires through a low-cost printing approach. It was found that response speed
can be regulated by adjusting the surface/volume (S/V) ratio of PEDOT: PSS. The fastest
response (<3.5 s) was achieved by using nanowires with a maximum S/V ratio. Besides,
by doping PEDOT: PSS nanowires with Graphene oxide (GO), its thermo-sensitivity can
be maximized at specific doping ratio. The optimized nanowires-based temperature
sensor was further integrated as a flexible epidermal electronic system (FEES) by
connecting with wireless communication components. Benefited by its flexibility, fast
and sensitive response, the FEES was demonstrated as a facile tool for different mobile
healthcare applications.
Keywords: temperature sensor, nanowires, fast response, healthcare, tumor, smartphone
INTRODUCTION
Real-time and continuous measurement of human body local epidermal temperature enables a
better tracking of personal health status such as local wounds infection (Celeste et al., 2013),
subcutaneous tumor (Sudharsan et al., 1999), as well as monitoring of body activities, since many
diseases and physiological behaviors will cause local changes in body epidermal temperature (Deng
and Liu, 2004; Helmy and Rizkalla, 2008; Ng, 2009; Li et al., 2017). Recently, wearable epidermal
electronic systems (EESs) based on flexible devices have opened new frontiers in the measurement
of body local temperature (Gao et al., 2014; Takei et al., 2015). Due to their soft and flexible nature,
they can be directly attached to the human skin and conform to the body, local temperature can

Zhou et al. Skin-Attachable Temperature Sensor
be detected anytime and anywhere (Webb et al., 2013; Zhang
et al., 2016). Besides, the use of soft substrate enables high
mechanical durability in different bending conditions, thus
their responses will not be influenced by the movement of
the body (Wu and Haick, 2018; Chang et al., 2019). However,
due to the materials limitation, current EESs based thermal
meters still suffer from the issues of responding slowly or not
sensitive enough to body temperature change, which in fact
cannot provide real-time precise temperature tracking. Hence the
development of fast and sensitive response wearable temperature
sensors which can track personal health status is still required.
Among all EES temperature sensor, PEDOT: PSS based
resistor-type electronics have been largely applied since the
PEDOT: PSS itself is very sensitive to temperature changes
(Culebras et al., 2016) and the soft nature of such organic
electronics ensures its excellent performance as flexible sensors
(Lipomi et al., 2012). The thermosensitive mechanism of PEDOT:
PSS can be explained by the structural change of PEDOT: PSS
induced by the temperature change which eventually alters the
conductivity of PEDOT: PSS (Takano et al., 2012; Zhou et al.,
2014; Vuorinen et al., 2016). Previous studies on PEDOT: PSS
based temperature sensors were focused on doping the PEDOT:
PSS with other materials to enhance the device’s response to
temperature (Honda et al., 2014; Oh et al., 2018). However,
understanding the control parameters regarding their response
time to temperature change is less covered.
In this work, in order to simultaneously optimize the
response speed and sensitivity of conductive polymers for
epidermal temperature sensing applications such as quick
temperature detecting or real-time precise temperature tracking.
we proposed a strategy to combine the micro/nano confinement
with the materials doping to simultaneously optimize the
response time and sensitivity of PEDOT: PSS based resistor-
type temperature sensor. Low dimension PEDOT: PSS wires
from a few micrometers down to sub-100 nm in diameters were
fabricated using a low-cost micro/nanoscale printing approach
(Gates et al., 2005; Massi et al., 2006; Duan et al., 2010;
Tang et al., 2019). Their sensitivity and response time to
temperature were compared (Scheme 1). Then, graphene oxide
(GO) was selected to dope the PEDOT: PSS and the doping
ratios were carefully optimized to enhance their temperature
sensing performance. Hence the fabricated sensor under such
strategy is responding both fast and sensitive enough to detective
minute temperature change and track temperature in real-time.
The sensor shows ultra-fast response and sensitive to body
temperature change. Furthermore, the sensor is also used to
achieve temperature monitoring of subcutaneous tumors in
mice and by detecting the minute change of body temperature
in mice to test the effect of drugs. Given the prominent
mechanical and sensing properties, a homemade wearable system
based on the temperature sensor was further developed to
achieve a live and wireless transmission of the signals to a
smartphone using Bluetooth assisted communication. These
results demonstrate that this fast response skin-attachable
nanowires-based temperature sensor has great potential as a
wearable bioelectronic for application in medical diagnosis and
mobile healthcare.
EXPERIMENTAL METHODS
Reagents and Materials
mr-I T85 was purchased from Micro-Resist. PEDOT: PSS
aqueous suspension (∼1.3 wt%) with a conductivity of 1 S cm−1
was purchased from Sigma-Aldrich. GO was purchased from
Chengdu Organic Chemical company and further sonicated
for 30 min to form a uniform and stable dispersion with
a concentration of 7 mg/ml. The compound solution was
obtained by stirring PEDOT: PSS aqueous suspension and GO
aqueous suspension for 10 min. Polydimethylsiloxane (PDMS)
was purchased from Dow corning.
Fabrication of Flat PDMS Molds With
Micro/Nano Grooves
First, casting the liquid prepolymer of PDMS base and the curing
agent in a 10:1 (w/w) ratio onto a silicon wafer with two kinds
of silicon micro-ridges (3 µm in width and 1 µm in height and
spacing 5 µm, 5 µm in width and 1 µm in height and spacing
10 µm, respectively). After the bubbles generated during the
stirring process disappear, the wafer with the uncured PDMS was
put into hot oven. After curing at 80◦C for 40 min, the PDMS
with microgrooves was cooled to room temperature and peeled
off from the silicon wafer. Then, the PDMS with microgrooves
was cut into pieces with the boundary of the microgrooves. The
fabrication of the molds with nanogroove can be seen on previous
case articles performed in our lab (Tang et al., 2019).
Formation of Micro/Nano Channels
The molds with micro/nano groove were first treated with oxygen
plasma (10 mTorr;10 sccm O2; 10 W; 15 s) to facilitate the contact
between the molds and PET substrates. The molds were then
bonded to the PET substrates which were also treated with
oxygen plasma (20 mTorr;20 sccm O2; 20W; 15s). The molds
can conformal contact with the PET substrates because of the
oxygen plasma treated procedure and soft properties of the molds
and PET substrates. Hence the micro/nano grooves changed into
micro/nano channels after contacting.
Electrodes Fabrication
The Au electrodes were then prepared by thermal evaporation
on the PET substrate with nanowires under self-made copper
shadow masks to promote the electrical connection. The
electrodes were with pad length in 7 mm, width in 300 µm
and spacing in 300 µm. The electrodes of microwires-based
devices were silver paste at an interval of 3 mm approximately.
Silver paste and silver wires were used to have further
electrical contacts.
Measurements
Atomic force microscope (AFM), Scanning electron microscope
(SEM) and the confocal laser scanning microscope (CLSM)
images were carried out with Dimension Icon (Bruker), FEI
FP 2031/12 Inspect F50 and OLYMPUS OLS5000, respectively.
Electrical measurements with a constant voltage of +1 V
were performed with a semiconductor analyzer (Agilent
Technologies, B1500A).
Frontiers in Chemistry | www.frontiersin.org 2March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
SCHEME 1 | Morphological model shows the different S/V ratio of PEDOT: PSS (A) microwires and (B) nanowire. Morphological model of the (C) thermosensitive and
(D) doping mechanism of PEDOT: PSS. (E) Carton shows the fabrication process of micro/nanowires.
Animal Tumor Model
Liver cancer tumor cells was injected into KM mice to establish
an animal tumor model.
Temperature Monitoring Based on
Smartphone
The homemade wearable watch-type system was
fabricated by integrating the AD5933/STM32/HC-05
and their peripheral circuits on a flexible circuit board.
AD5933/STM32/HC-05 control resistance measurement,
communication, and data transmission, respectively.
An Android application program was developed on
the smartphone to receive real-time data from the
wearable watch-type system and plot the responses on the
screen. Comparing the response change to its resistance
calibration at standard temperature, the temperature was
successfully measured.
RESULTS AND DISCUSSION
Micro/nanowires Fabrication and
Characterization
To study the structure effects on the thermal sensing performance
of PEDOT: PSS, here we design three different sized PEDOT:
PSS wires, where their widths vary from 4 µm to 70 nm
(Scheme 1). Hence different S/V ratios are achieved. The
micro/nanowires were fabricated by an adapted soft lithography
which does not require any cleanroom facilities (Gates et al.,
2005; Massi et al., 2006; Duan et al., 2010; Tang et al., 2019).
Scheme 1E shows the schematic of fabricating procedure
Frontiers in Chemistry | www.frontiersin.org 3March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
FIGURE 1 | (A) Optical microscope, (B) SEM, (C) AFM, and (D) CLSM, image of microwires @ 4µm. (E) Optical microscope, (F) SEM, (G) AFM, and (H) CLSM,
image of microwires @ 2 µm. (I) Optical microscope, (J) SEM, (K) AFM, and (L) CLSM, image of nanowires.
of micro/nanowires. After the micro/nanochannels (The
preparation process is shown in the Experimental Methods)
have completely formed, the PEDOT: PSS aqueous solution
were dropped to the margins of channels. The solution filled
the channels spontaneously by traction of the Laplace pressure.
After the solvent has completely evaporated, removed the
mold from PET and leaved the micro/nanowires on the PET
substrate. Then, metal electrodes were fabricated on the side
of the micro/nanowires through evaporation as the contact
electrodes, thus resistor-type sensors have been achieved. The
comparison between our method and current available methods
for fabricating nanowires in the format of a table is shown in
Supplementary Information.
Figure 1 shows the optical microscope, Scanning Electron
Microscope (SEM), Atomic Force Microscope (AFM) and
Confocal Laser Scanning Microscope (CLSM) images of the
micro/nanowires with different sizes, respectively. These results
show that the microwires have the same height (∼0.7 µm)
but with different width (4 µm, 2 µm). The nanowires have
an average width of 70 nm and an average height of 59 nm.
Thus, the S/V ratio of microwires @ 4 µm, microwires @
2µm and nanowires can be calculated as follow: 1.928, 2.429,
and 45.52. As can be seen in the AFM images, the height
of the microwires sides are higher than the middle part,
which is due to the microchannels are treated with O2plasma
hence are more hydrophilic, thus the aqueous solution tends
to stick to the wall before evaporates, which resulting in
this phenomenon.
Temperature Sensing
To study the structure effects on their temperature sensing
behavior, we compared the response value and response speed
of the three PEDOT: PSS based resistor-type temperature sensors
with different S/V ratio. Their resistance were measured under
a temperature range from 30 to 80◦C with an interval of 10◦C
(Figures 2A–C). The response value is defined as:
δR=((R−R0)/R0
)
where R0and R are the resistance values at 30◦C
and the set temperature. And TCR is defined as
TCR =((R−R0)/R0)/1T=δR/1T. The results show
that the resistance of the three devices decrease linearly as
the temperature rises and their sensitivity (slope of the liner
fitting) are rather similar (Figure 2D). The δR of PEDOT: PSS
microwires @ 4 µm, microwires @ 2 µm and nanowires-based
temperature sensor between 30 and 80◦C (303 and 353 K)
are −0.377, −0.378, and −0.379, so the TCR of them can
be calculated as −0.007545, −0.007579, and −0.007599 K−1.
We then tested their response speed to temperature change
by attaching or removing these devices to human arm which
has a constant temperature. As shown in Figures 2E–G, the
currents show increase or decrease after touching or removing
the devices from the human skin. Compare with their thermal
sensitivity, very differently, the devices with different S/V ratio
show quite different temperature response speed (defined as the
Frontiers in Chemistry | www.frontiersin.org 4March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
FIGURE 2 | Relative resistance changes depending on the temperature with increments of 10◦C of the (A) microwires @ 4µm, (B) microwires @ 2 µm and (C)
nanowires, based temperature sensor. (D) Sensitivity of the sensors with different S/V ratio. Real-time response of (E) microwires @ 4µm, (F) microwires @ 2 µm and
(G) nanowires, based temperature sensor. (H) Total response time of the sensors with different S/V ratio.
time required to reach 90% of the zenith response). The response
and recovery time of the microwires @ 4 µm, microwires @
2µm and nanowires-based temperature sensor were 6.9 and
25.2 s, 5.8 and 23.8 s, 3.5 and 13.4 s, respectively. As compared
in Figure 2H, a clear trend can be observed that the response
speed increases with the increase of the S/V ratio, especially
the nanowires with a maximum S/V ratio shows an ultra-fast
response speed. This behavior can be explained by the electron
transportation and thermal sensing mechanism of PEDOT:
PSS which is very related to its microstructure. As shown in
Scheme 1C, PEDOT: PSS has a typical core-shell structure
in which the core is PEDOT nanocrystal and surrounded by
PSS-rich shell. The insulating PSS boundaries with a strong
hygroscopic ability have a major effect to the overall conductance
of the PEDOT: PSS (Takano et al., 2012; Zhou et al., 2014). When
temperature rising, the water molecules absorbed in the PSS
boundaries will be partially released, which leads to the shrinkage
of PSS boundaries and results in a decrease of the distance
between adjacent PEDOT (Scheme 1C). This will facilitate the
electron transportation between the PEDOT domains and results
the decrease of the resistance of PEDOT: PSS (Zhou et al., 2014;
Vuorinen et al., 2016). The response of PEDOT: PSS film are
shown in Figure S1 in Supplementary Information. By confining
the PEDOT: PSS from 2D thin film to 1D nanowire (increase
of its S/V ratio), PSS boundaries can be fully exposed to the
external environment, thus increase its thermal conduction
and facilitates the water evaporation, which will increase its
response speed to temperature change. Besides, the electron
transport efficiency within the 1D nanowire is improved as well.
Other nanomaterials-based resistive temperature sensors also
have showed such advantages of nanomaterials in temperature
detecting (Joh et al., 2018; Sehrawat et al., 2018; Bang et al., 2019;
Cui et al., 2019). However, reducing the materials dimension
will not influence the deformation ratio of the PSS boundaries,
which is related to the amount of the water absorbed, thus the
change of S/V ratio will not influence the thermal sensitivity of
PEDOT: PSS.
Doping Effect
As discussed above, nanoscale confinement strategy can enhance
the response speed of the PEDOT: PSS to temperature and
PEDOT: PSS nanowires with the highest S/V ratio show the
fattest response to temperature change which is rather important
to develop as temperature sensor. Next, we focus on improving
its thermal sensitivity. As reported before, doping of PEDOT:
PSS with other temperature-sensitive materials such as graphene
(Trung et al., 2014, 2016, 2018) can further increase its response
to temperature (Honda et al., 2014; Oh et al., 2018). Here,
we applied the graphene doping strategy to further adjust the
temperature sensitivity of PEDOT: PSS nanowires. Since the
mixtures are required to be dispersed in aqueous solution for
capillary filling, the oxidation form of graphene (GO) was used,
which contains many oxygen-containing functional groups, such
as hydroxyl, epoxide and carboxyl groups and ensures its good
solubility in aqueous solution (Wang et al., 2009; Chen and
Li, 2012; Lee et al., 2012; Dwandaru et al., 2019). The doped
mixtures were characterized by FT-IR (Figure S2 in Supporting
Information), the mixtures have the same characteristics as
PEDOT: PSS and contain the specific bands of GO, which proves
that the two materials have been fully mixed and the chemical
structures of PEDOT: PSS and GO are well-maintained. We then
optimized the GO doping ratio to understand its thermal sensing
effect. I–V curves of the nanowires constructed by mixtures with
different mixing ratios (PEDOT: PSS/GO, V/V) were measured
under temperature range from 30 to 80◦C with an interval of
10◦C. As shown in Figure 3A, the GO doping has a conspicuous
influence on the thermal sensitivity of the PEDOT: PSS. The
nanowire device with mixing ratio of 13:1 shows the highest
temperature response. This can be explained by the fact that GO
is a kind of relatively hydrophilic material, thus GO should be
Frontiers in Chemistry | www.frontiersin.org 5March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
FIGURE 3 | (A) Relative resistance changes of the sensors with different mixing ratios at different temperatures. (B) Schematic diagram of PEDOT: PSS nanowires
doped with opportune, insufficient and excessive amount of GO; Real-time response of the nanowire sensors with a mixing ratio of (C) 13:1 and (D) 20:1, after
attached to and removal off the human arm.
mostly adsorbed on the hydrophilic PSS when it is mixed with
PEDOT: PSS. Hence a little bit of GO will not affect the overall
conductivity of PEDOT: PSS due to PSS does not participate in
conductivity of PEDOT: PSS. However, GO has excellent thermal
conductivity (Teng et al., 2011; Yao et al., 2016), hence doping
GO can affect the thermal sensitivity of PEDOT: PSS. When the
mixing ratio is 13:1 (The upper schematic of Figure 3B), the
GO flakes are fully filled in the PSS and the gap between the
adjacent PEDOT: PSS nanoparticles. Such composite materials
show higher temperature sensitivity compared to the less, more
or no GO filling. If the mixing ratio is higher than 13:1, such as
15:1, which means the amount of GO flakes is less than that of
13:1, hence the GO flakes are not adequately filled in the PSS and
the gap between adjacent PEDOT: PSS nanoparticles(The middle
schematic of Figure 3B), leading to the temperature sensitivity
of this ratio lower than that of 13:1 but higher than non-doped
pure PEDOT: PSS. If the mixing ratio is lower than 13:1, such
as 10:1, under such mixing ratio, the amount of GO is larger
than that of 13:1, hence the connection between adjacent PEDOT:
PSS nanoparticles will be affected (The bottom schematic of
Figure 3B), leading to the response of this ratio lower than that of
13:1. Furthermore, when the ratio is further reduced, such as 1:1,
which means the proportion of GO is far more than that of 13:1,
hence the connection between the PEDOT: PSS nanoparticles
will be affected severely, leading to the response of this ratio
is even lower than that of non-doped pure PEDOT: PSS. We
also explored whether the GO doping would affect the response
speed of PEDOT: PSS nanowires. As shown in Figures 3C,D,
compared with the pure PEDOT: PSS nanowires (Figure 2E), the
response time and recovery time of these GO doped nanowires
have no obvious difference. It proves that the GO doping did
not affect the response speed of PEDOT: PSS nanowires but
only enhance the thermal sensitivity. Thus, by combining the
nanoconfinement and GO doping strategy, the response speed
and thermal sensitivity can be simultaneously optimized. The
13:1 GO doped nanowires are used to prepare the temperature
sensor for rest of the applications.
Repeatability and Stability
After optimization the structure and the materials, we then
fabricated the optimized Go doped PEDOT: PSS nanowires on
a flexible PET substrate to facilitate their epidermal sensing
applications. The repeatability and stability of the nanoscale
flexible sensors were tested, especially for their hysteretic
behavior (Han et al., 2018). Figure 4A shows the hysteresis of the
nanowires response to temperature with a heating and cooling
cycle, which indicates a very minor hysteresis (∼0.0046). Next,
we evaluated the repeatability of the nanowires-based sensor by
applying the sensor for multiple tests of touch to and removal
from the skin (Figure 4B). The stable performance demonstrates
that the devices have good repeatability and stability. The sensors
were then kept under ambient air for 1 months and their
response to temperature change were measured again. The
results in Figure S3 in the Supporting Information show that
their temperature response after 1 months is slightly changed
Frontiers in Chemistry | www.frontiersin.org 6March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
FIGURE 4 | (A) Relative resistance changes depending on the temperature with increments/decrements of 1◦C. (B) Real-time response of a nanowire sensor after
attached to and removal off the human arm for three times.
FIGURE 5 | (A) IR thermograms and picture(middle) of the temperature sensor attached on the head of five volunteers. Resistance of the device and measured skin
temperature of (B) five volunteers and (C) a volunteer before and after 30 push-ups.
in comparison with the as-fabricated sensors, which prove the
long-term stability of the PEDOT: PSS nanowires in ambient air.
Skin Temperature Detection
We then tested the nanowires-based temperature sensor for
skin temperature detection. Five volunteers were chosen to
use the sensors for monitoring their local skin temperature by
attaching these devices on their heads (Figure 5A). The good
mechanical property and ultra-thin size of the flexible sensor
facilitate its attachment to human skin and hence ensure the
reliable temperature measurement. According to the results of
the previous fitting, the corresponding skin temperature of five
volunteers can be calculated. As shown in Figure 5B, the skin
temperature of the five volunteers is 35.12◦C, 34.86◦C, 34.71◦C,
35.05◦C, 35.36◦C, respectively. The results are consistent with
the results obtained by thermocouple which proves the accuracy
of the device (35.1◦C, 34.7◦C, 34.7◦C, 35.0◦C, 35.2◦C). Since
the skin temperature will change during strenuous or long-term
exercise, we apply the temperature sensor to track the volunteer
exercise status. The sensor was attached to the head of a volunteer
to monitor the subtle temperature changes during exercise. The
normal skin temperature of the volunteer’s temple was measured
to be approximately 34.93◦C. It increased to approximately
35.37◦C after doing 30 push-ups (see Figure 5C). These results
demonstrate that the nanowire-based temperature sensors can be
effectively applied for rapidly and accurately tracking of human
skin temperature.
Mobile Healthcare Based on Nanoscale
Fees
Many diseases and physiological behaviors will cause local
changes in body epidermal temperature, hence real-time and
continuous measurement of the local skin temperature could
enable a better tracking of personal health status (Deng and
Liu, 2004; Helmy and Rizkalla, 2008; Ng, 2009; Li et al.,
2017). Based on the nanoscale flexible temperature sensor,
a wearable FEES was further developed by integrating the
nanowires with commercial electronic components to enable
the wireless communication. An Android application program
was further developed and installed on a smartphone to
directly receive and process the sensing signals in real-
time. As shown in Figure S4, the FEES can be worn on
the wrist for continuously monitoring the skin temperature.
Figure 6A shows the screenshot of the smartphone interacting
with the FEES system by touching or removing the system
from the skin, which demonstrates their rapid response to
Frontiers in Chemistry | www.frontiersin.org 7March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
FIGURE 6 | A screenshot of the smartphone when the sensor was attached on (A) a human arm, (B) a mouse after intraperitoneal injection of adrenaline and a
mouse after hypodermic injection of adrenaline. (C) Picture of the mouse with a subcutaneous tumor. (D) Skin temperature distribution of subcutaneous tumor and
eight points near it measured by the nanowires-based EES.
human skin temperature. The system was further applied to
compare the administration route of drugs by monitoring
the subtle skin temperature changes after intraperitoneal and
hypodermic injection of adrenaline to a mouse (Figure 6B). It
clearly shows that after intraperitoneal injection of adrenaline,
the resistance of the device did not change significantly,
indicating that body temperature of the mouse was constant.
While after hypodermic injection, the resistance of the sensor
was slowly and continuously decreased, indicating that body
temperature of the mouse was slowly increasing, which are
consistent with the existing studies (Maling et al., 1979). These
results demonstrate the feasibility of the FEES system in real
temperature monitoring applications.
Subcutaneous tumors, as a kind of common tumor, will
change the metabolic activity of the lesion area and in turn
change the normal temperature distribution on the skin surface
(Sudharsan et al., 1999). Benefited by the fast response and
high thermal sensitivity, the EES could provide a neat tool to
monitoring skin temperature outside the subcutaneous tumors
in a new way. Figure 6D shows the skin temperature distribution
around the tumor area detected by attaching the FEES on
different place of the skin (Figure 6C). The results indicate that
the temperature in the tumor area is significantly lower than
the surrounding area, which is consistent with the results of
existing studies (Konerding and Steinberg, 1988). Meanwhile,
the results detected by the FEES are more accurate than IR
thermograms (inset in Figure 6C), and this method provides
the possibility of real-time monitoring. It also shows that the
sensor has great potential to be made into temperature sensor
arrays, which can detect spatial mapping of skin temperature
so that the arrays could provide a feasible method to judge
the diffusion area and monitor the deterioration status of
the subcutaneous tumors efficiently and conveniently. All
these results demonstrate that this EES has great potential
as a wearable bioelectronic for mobile medical diagnosis and
healthcare applications.
CONCLUSION
In this work, we developed a strategy by combining the
micro/nano confinement with materials doping to enable
simultaneous optimization of the response speed and sensitivity
of low dimension conductive polymers. By confining the PEDOT:
PSS into nanowires and doping with GO at optimized doping
ratio, ultra-fast response to temperature change (<3.5 s) and
maximized thermal-sensitivity is achieved. Well-defined sub-
100 nm nanowires were fabricated on flexible substrates using
a low-cost nanoscale printing approach which were further
integrated as a functional skin-attachable flexible epidermal
electronic system (FEES) to enable a live and wireless
temperature sensing. The developed FEES were applied for
different physiological behaviors and diseases monitoring by
recording the real-time skin temperature changes.
DATA AVAILABILITY STATEMENT
All datasets generated for this study are included in the
article/Supplementary Material.
Frontiers in Chemistry | www.frontiersin.org 8March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
ETHICS STATEMENT
The animal study was reviewed and approved by the ethics
committee of the Institute of Radiation Medicine Chinese
Academy of Medical Sciences.
AUTHOR CONTRIBUTIONS
CZ developed the ideas of the study, carried out most of the
experiments, and also wrote most parts of the manuscript. NT
and XZ also developed some ideas of the study and participated in
some experiments, and also reviewed the manuscript. YF, YJ, and
HZ participated in some experiments of the study and reviewed
the manuscript. XD developed some ideas and improved the
ideas other authors developed and also wrote parts of the
manuscript. All authors read and approved the final manuscript.
FUNDING
This work was supported by National Natural Science
Foundation of China (NSFC Nos. 61674114, 91743110,
21861132001), National Key R&D Program of China
(2017YFF0204604, 2018YFE0118700), Tianjin Applied Basic
Research and Advanced Technology (17JCJQJC43600), the
Foundation for Talent Scientists of Nanchang Institute
for Microtechnology of Tianjin University, and the 111
Project (B07014).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fchem.
2020.00194/full#supplementary-material
REFERENCES
Bang, J., Lee, W. S., Park, B., Joh, H., Woo, H. K., Jeon, S., et al. (2019).
Highly sensitive temperature sensor: ligand-treated ag nanocrystal thin films
on PDMS with thermal expansion strategy. Adv. Functional Mater. 29:1903047.
doi: 10.1002/adfm.201903047
Celeste, C. J., Deschesne, K., Riley, C. B., and Theoret, C. L. (2013). Skin
temperature during cutaneous wound healing an equine model of cutaneous
fibroproliferative disorder: kinetics and anatomic-site differences. Vet. Surg. 42,
147–153. doi: 10.1111/j.1532-950X.2012.00966.x
Chang, Y., Zuo, J., Zhang, H., and Duan, X. (2019). State-of-the-art and
recent developments in micro/nanoscale pressure sensors for smart wearable
devices and health monitoring systems. Nanotechnol. Eng. 3, 43–52.
doi: 10.1016/j.npe.2019.12.006
Chen, F., and Li, J. H. (2012). Graphene oxide: preparation, functionalization,
and electrochemical applications. Chem. Rev. 112, 6027–6053.
doi: 10.1021/cr300115g
Cui, Z., Poblete, F. R., and Zhu, Y. (2019). Tailoring the temperature coefficient
of resistance of silver nanowire nanocomposites and their application as
stretchable temperature sensors. ACS Appl. Mater. Interface 11, 17836–17842.
doi: 10.1021/acsami.9b04045
Culebras, M., López, A. M., Gómez, C. M., and Cantarero, A. (2016). Thermal
sensor based on a polymer nanofilm. Sens. Actuators A Phys. 239, 161–165.
doi: 10.1016/j.sna.2016.01.010
Deng, Z. S., and Liu, J. (2004). Mathematical modeling of temperature mapping
over skin surface and its implementation in thermal disease diagnostics.
Comput. Biol. Med. 34, 495–521. doi: 10.1016/S0010-4825(03)00086-6
Duan, X., Zhao, Y., Berenschot, E., Tas, N. R., Reinhoudt, D. N., and
Huskens, J. (2010). Large-area nanoscale patterning of functional
materials by nanomolding in capillaries. Adv. Funct. Mater. 20, 2519–2526.
doi: 10.1002/adfm.201000492
Dwandaru, W. S. B., Parwati, L. D., and Wisnuwijaya, R. I. (2019). Formation of
graphene oxide from carbon rods of zinc-carbon battery wastes by audiosonic
sonication assisted by commercial detergent. Nanotechnol. Eng. 2, 89–94.
doi: 10.1016/j.npe.2019.03.001
Gao, L., Zhang, Y. H., Malyarchuk, V., Jia, L., Jang, K. I., Webb, R. C., et al.
(2014). Epidermal photonic devices for quantitative imaging of temperature
and thermal transport characteristics of the skin. Nat. Commun. 5:4938.
doi: 10.1038/ncomms5938
Gates, B. D., Xu, Q., Stewart, M., Ryan, D., Willson, C. G., and Whitesides, G.
M. (2005). New approaches to nanofabrication: molding, printing, and other
techniques. Chem. Rev. 105, 1171–1196. doi: 10.1021/cr030076o
Han, S., Liu, Q., Han, X., Dai, W., and Yang, J. (2018). An E-type
temperature sensor for upper air meteorology. Nanotechnol. Eng. 1, 145–149.
doi: 10.13494/j.npe.20170016
Helmy, H., and Rizkalla, M. (2008). Application of thermography for non-invasive
diagnosis of thyroid gland disease. IEEE Trans. Biomed. Eng. 55, 1168–1175.
doi: 10.1109/TBME.2008.915731
Honda, W., Harada, S., Arie, T., Akita, S., and Takei, K. (2014). Printed wearable
temperature sensor for health monitoring. IEEE Sens. Proc. 2014, 2227–2229.
doi: 10.1109/ICSENS.2014.6985483
Joh, H., Lee, W. S., Kang, M. S., Seong, M., Kim, H., Bang, J., et al.
(2018). Surface design of nanocrystals for high-performance multifunctional
sensors in wearable and attachable electronics. Chem. Mater. 31, 436–444.
doi: 10.1021/acs.chemmater.8b03914
Konerding, M. A., and Steinberg, F. (1988). Computerized infrared thermography
and ultrastructural studies of xenotransplanted human tumors on nude mice.
Thermology 3, 7–14.
Lee, K. D., You, J. M., Kim, S. K., and Yun, M., Jeon, S. (2012). Electrocatalytic
oxidation of hydrazine and hydroxylamine by graphene oxide-Pd nanoparticle-
modified glassy carbon electrode. J. Nanosci. Nanotechnol. 12, 8886–8892.
doi: 10.1166/jnn.2012.6792
Li, Q. L., Zhang, N. X.,Tao, M., and Ding, X. (2017). Review of flexible temperature
sensing networks for wearable physiological monitoring. Adv. Healthcare.
Mater. 6, 1–23. doi: 10.1002/adhm.201601371
Lipomi, D. J., Lee, J. A., Vosgueritchian, M., Tee, B. C. K., Bolander, J. A., and Bao,
Z. (2012). Electronic properties of transparent conductive films of PEDOT:PSS
on stretchable substrates. Chem. Mater. 24, 373–382. doi: 10.1021/cm203216m
Maling, H. M., Williams, M. A., and Koppanyi, T. (1979). Salivation in mice as
an index of adrenergic activity. Salivation, I., and temperature responses to
d-amphetamine and other sialogogues and the effects of adrenergic blocking
agents. Arch. Int. Pharmacodyn. Ther. 199, 318–332.
Massi, M., Albonetti, C., Facchini, M., Cavallini, M., and Biscarini, F. (2006).
Toward amorphous conductors: enhanced conductivity of doped polyaniline
via interchain crosslinking promoted by acid-functionalized aluminum
quinolines. Adv. Mater. 18, 2739–2742. doi: 10.1002/adma.200600465
Ng, E. Y. K. (2009). A review of thermography as promising non-invasive
detection modality for breast tumor. Int. J. Therm. Sci. 48, 849–859.
doi: 10.1016/j.ijthermalsci.2008.06.015
Oh, J. H., Hong, S. Y., Park, H., Jin, S. W., Jeong, Y. R., Oh, S. Y., et al.
(2018). Fabrication of high-sensitivity skin-attachable temperature sensors
with bioinspired microstructured adhesive. ACS Appl. Mater. Interfaces 10,
7263–7270. doi: 10.1021/acsami.7b17727
Sehrawat, P., Islam, S. S., and Mishra, P. (2018). Reduced graphene oxide
based temperature sensor: extraordinary performance governed by lattice
dynamics assisted carrier transport. Sens. Actuators B Chem. 258, 424–435.
doi: 10.1016/j.snb.2017.11.112
Sudharsan, N. M., Ng, E. Y. K., and Teh, S. L. (1999). Surface temperature
distribution of a breast with and without tumour. Comput. Methods Biomech.
Biomed. Eng. 2, 187–199. doi: 10.1080/10255849908907987
Frontiers in Chemistry | www.frontiersin.org 9March 2020 | Volume 8 | Article 194

Zhou et al. Skin-Attachable Temperature Sensor
Takano,T., Masunaga, H., Fujiwara, A., Okuzaki, H., and Sasaki, T. (2012). PEDOT
nanocrystal in highly conductive PEDOT: PSS polymer films. Macromolecules
45, 3859–3865. doi: 10.1021/ma300120g
Takei,K., Honda, W., Harada, S., Arie, T., and Akita, S. (2015). Toward flexible and
wearable human-interactive health-monitoring devices. Adv. Healthcare Mater.
4, 487–500. doi: 10.1002/adhm.201400546
Tang, N., Zhou, C., Xu,L., Jiang, Y., Qu, H., and Duan, X. (2019). A fully integrated
wireless flexible ammonia sensor fabricated by soft nano-lithography. ACS Sens.
4, 726–732. doi: 10.1021/acssensors.8b01690
Teng, C. C., Ma, C. M., Lu, C. H., Yang, S. Y., Lee, S. H., Hsiao, M.
C., et al. (2011). Thermal conductivity and structure of non-covalent
functionalized graphene/epoxy composites. Carbon 49, 5107–5116.
doi: 10.1016/j.carbon.2011.06.095
Trung, T. Q., Le, H. S., Dang, T. M. L., Ju, S., Park, S. Y., and Lee, N. E.
(2018). Freestanding, fiber-based, wearable temperature sensor with tunable
thermal index for healthcare monitoring. Adv. Healthc. Mater. 7, 1–9.
doi: 10.1002/adhm.201800074
Trung, T. Q., Ramasundaram, S., Hong, S. W., and Lee, N. E. (2014). Flexible
and transparent nanocomposite of reduced graphene oxide and P(VDF-TrFE)
copolymer for high thermal responsivity in a field-effect transistor. Adv. Funct.
Mater. 24, 3438–3445. doi: 10.1002/adfm.201304224
Trung, T. Q., Ramasundaram, S., Hwang, B. U., and Lee, N. E. (2016). An all-
elastomeric transparent and stretchable temperature sensor for body-attachable
wearable electronics. Adv. Mater. 28, 502–509. doi: 10.1002/adma.2015
04441
Vuorinen, T., Niittynen, J., Kankkunen, T., Kraft, T. M., and Mäntysalo, M.
(2016). Inkjet-printed graphene/PEDOT: PSS temperature sensors on a skin-
conformable polyurethane substrate. Sci. Rep. 6, 1–8. doi: 10.1038/srep35289
Wang, Y., Li, Y., Tang, L., Lu, J., and Li, J. (2009). Application of graphene-
modified electrode for selective detection of dopamine. Electrochem. Commun.
11, 889–892. doi: 10.1016/j.elecom.2009.02.013
Webb, R. C., Bonifas, A. P., Behnaz, A., Zhang, Y., Yu, K. J., Cheng, H.,
et al. (2013). Ultrathin conformal devices for precise and continuous
thermal characterization of human skin. Nat. Mater. 12, 938–944.
doi: 10.1038/nmat3755
Wu, W., and Haick, H. (2018). Materials and wearable devices for
autonomous monitoring of physiological markers. Adv. Mater. 30:1705024.
doi: 10.1002/adma.201705024
Yao, Y., Zeng, X., Wang, F., Sun, R., Xu, J. B., and Wong, C. P. (2016).
Significant enhancement of thermal conductivity in bioinspired freestanding
boron nitride papers filled with graphene oxide. Chem. Mater. 28, 1049–1057.
doi: 10.1021/acs.chemmater.5b04187
Zhang, Y. H., Webb, R. C., Luo, H. Y., Xue, Y. G., Kurniawan, J., Cho, N. H., et al.
(2016). Theoretical and experimental studies of epidermal heat flux sensors for
measurements of core body temperature. Adv. Healthcare Mater. 5, 119–127.
doi: 10.1002/adhm.201500110
Zhou, J., Anjum, D. H., Chen, L., Xu, X., Ventura, I. A., Jiang, L., et al. (2014).
The temperature-dependent microstructure of PEDOT/PSS films: insights
from morphological, mechanical and electrical analyses. J. Mater. Chem. C 2,
9903–9910. doi: 10.1039/C4TC01593B
Conflict of Interest: The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be construed as a
potential conflict of interest.
Copyright © 2020 Zhou, Tang, Zhang, Fang, Jiang, Zhang and Duan. This is an
open-access article distributed under the terms of the Creative Commons Attribution
License (CC BY). The use, distribution or reproduction in other forums is permitted,
provided the original author(s) and the copyright owner(s) are credited and that the
original publication in this journal is cited, in accordance with accepted academic
practice. No use, distribution or reproduction is permitted which does not comply
with these terms.
Frontiers in Chemistry | www.frontiersin.org 10 March 2020 | Volume 8 | Article 194