A Skin-Inspired Self-Adaptive System for Temperature Control During Dynamic Wound Healing

doi:10.1007/s40820-024-01345-0

Abstract

Abstract:

The thermoregulating function of skin that is capable of maintaining body temperature within a thermostatic state is critical. However, patients suffering from skin damage are struggling with the surrounding scene and situational awareness. Here, we report an interactive self-regulation electronic system by mimicking the human thermos-reception system. The skin-inspired self-adaptive system is composed of two highly sensitive thermistors (thermal-response composite materials), and a low-power temperature control unit (Laser-induced graphene array). The biomimetic skin can realize self-adjusting in the range of 35-42 °C, which is around physiological temperature. This thermoregulation system also contributed to skin barrier formation and wound healing. Across wound models, the treatment group healed ~ 10% more rapidly compared with the control group, and showed reduced inflammation, thus enhancing skin tissue regeneration. The skin-inspired self-adaptive system holds substantial promise for next-generation robotic and medical devices.

Key words: Thermo-reception, Self-regulation, Flexible electronic system, Wound healing

Yaqi Geng, Guoyin Chen, Ran Cao, Hongmei Dai, Zexu Hu, Senlong Yu, Le Wang, Liping Zhu, Hengxue Xiang, Meifang Zhu. A Skin-Inspired Self-Adaptive System for Temperature Control During Dynamic Wound Healing[J]. Nano-Micro Letters, 2024, 16(1): 152-.

Yaqi Geng, Guoyin Chen, Ran Cao, Hongmei Dai, Zexu Hu, Senlong Yu, Le Wang, Liping Zhu, Hengxue Xiang, Meifang Zhu. [J]. Nano-Micro Letters, 2024, 16(1): 152-.

/ / Recommend / Download Citations

URL: https://www.qk.sjtu.edu.cn/nml/EN/10.1007/s40820-024-01345-0

https://www.qk.sjtu.edu.cn/nml/EN/Y2024/V16/I1/152

Figures/Tables 5

Fig. 1 Design concepts and system features of the interactive thermo-regulation bionic electronic system (TRES). a Temperature self-regulation mechanism in homoiotherms. b The actual picture of TRES placed on the arm. c Temperature self-regulation mechanism of TRES. d Assembly diagram of TRES

Fig. 2 Preparation and Joule thermal properties of the LIG TC. a Preparation process of the LIG TC. b SEM image of LIG (texture structure and porous structure). c XPS analysis of LIG. d Joule thermal properties LIG TC. e The heating stability of the LIG TC

Fig. 3 Preparation and thermo-response properties of PTC thermistors. a Preparation process of PTC thermistors. b The stability of PTC ink. c Molecular formula of functional polymers. d Melting and crystallization capacity of acrylate copolymers. e Working mechanism of PTC thermistors. f Temperature response performance of PTC thermistors. g The response stability of PTC thermistors

Fig. 4 Circuit design and self-regulating performance of TRES. a Circuit diagram in normal working condition. b Schematic diagram of connection mode of protection circuit and feedback circuit. c Working mechanism of different thermistors. d Protection circuit diagram. e Real-time temperature during T2 working. f The temperature change of LIG TC on T2 working. g Feedback circuit diagram. h The temperature change of LIG TC on T1 working. i The indicator of oscilloscope changes in real time

Fig. 5 Evaluation of in vivo wound healing and histological analysis. a Illustruction of how TRES works in the wound. b Physical image of TRES placed on mice. c Thermal infrared imaging of mice heated by a TRES. d LIG TC and commercial heater monitor temperature in real-time. e Photographs of dorsal wounds of mice treated with nothing, commercial heater, and TRES. f The percentages of wound contraction in 12 days and the changes in the wound boundaries. g, h Histological analysis of the wounds treated via H&E staining and Masson staining (n = 3, p < 0.05)

References 47

1.	W.D. Li, K. Ke, J. Jia, J.H. Pu, X. Zhao et al., Recent advances in multiresponsive flexible sensors toward E-skin: a delicate design for versatile sensing. Small 18, e2103734 (2022). https://doi.org/10.1002/smll.202103734
2.	M. Wang, Y. Luo, T. Wang, C. Wan, L. Pan et al., Artificial skin perception. Adv. Mater. 33, 2003014 (2021). https://doi.org/10.1002/adma.202003014
3.	J.Y. Oh, Z. Bao, Second skin enabled by advanced electronics. Adv. Sci. 6, 1900186 (2019). https://doi.org/10.1002/advs.201900186
4.	A. Chortos, J. Liu, Z. Bao, Pursuing prosthetic electronic skin. Nat. Mater. 15, 937-950 (2016). https://doi.org/10.1038/nmat4671
5.	C. Wang, C. Pan, Z. Wang, Electronic skin for closed-loop systems. ACS Nano 13, 12287-12293 (2019). https://doi.org/10.1021/acsnano.9b06576
6.	L.E. Osborn, R. Venkatasubramanian, M. Himmtann, C.W. Moran, J.M. Pierce et al., Evoking natural thermal perceptions using a thin-film thermoelectric device with high cooling power density and speed. Nat. Biomed. Eng. (2023). https://doi.org/10.1038/s41551-023-01070-w
7.	S.R. Madhvapathy, J.J. Wang, H. Wang, M. Patel, A. Chang et al., Implantable bioelectronic systems for early detection of kidney transplant rejection. Science 381, 1105-1112 (2023). https://doi.org/10.1126/science.adh7726
8.	M. Jiang, Q. Shen, J. Zhang, S. An, S. Ma et al., Bioinspired temperature regulation in interfacial evaporation. Adv. Funct. Mater. 30, 1910481 (2020). https://doi.org/10.1002/adfm.201910481
9.	C.L. Tan, E.K. Cooke, D.E. Leib, Y.C. Lin, G.E. Daly et al., Warm-sensitive neurons that control body temperature. Cell 167, 47-59 (2016). https://doi.org/10.1016/j.cell.2016.08.028
10.	R. Dong, B. Guo, Smart wound dressings for wound healing. Nano Today 41, 101290 (2021). https://doi.org/10.1016/j.nantod.2021.101290
11.	D. Lou, Q. Pang, X. Pei, S. Dong, S. Li et al., Flexible wound healing system for pro-regeneration, temperature monitoring and infection early warning. Biosens. Bioelectron. 162, 112275 (2020). https://doi.org/10.1016/j.bios.2020.112275
12.	P. Tang, Y. Liu, Y. Liu, H. Meng, Z. Liu et al., Thermochromism-induced temperature self-regulation and alternating photothermal nanohelix clusters for synergistic tumor chemo/photothermal therapy. Biomaterials 188, 12-23 (2019). https://doi.org/10.1016/j.biomaterials.2018.10.008
13.	Y. Gao, H. Du, Z. Xie, M. Li, J. Zhu et al., Self-adhesive photothermal hydrogel films for solar-light assisted wound healing. J. Mater. Chem. B 7, 3644-3651 (2019). https://doi.org/10.1039/C9TB00481E
14.	G. Chen, K. Hou, N. Yu, P. Wei, T. Chen et al., Temperature-adaptive hydrogel optical waveguide with soft tissue-affinity for thermal regulated interventional photomedicine. Nat. Commun. 13, 7789 (2022). https://doi.org/10.1038/s41467-022-35440-w
15.	S. Zhao, R. Zhu, Electronic skin with multifunction sensors based on thermosensation. Adv. Mater. 29, 1606151 (2017). https://doi.org/10.1002/adma.201606151
16.	Y. Lee, J. Park, A. Choe, S. Cho, J. Kim et al., Mimicking human and biological skins for multifunctional skin electronics. Adv. Funct. Mater. 30, 1904523 (2020). https://doi.org/10.1002/adfm.201904523
17.	K. Kwon, J.U. Kim, S.M. Won, J. Zhao, R. Avila et al., A battery-less wireless implant for the continuous monitoring of vascular pressure, flow rate and temperature. Nat. Biomed. Eng. 7, 1215-1228 (2023). https://doi.org/10.1038/s41551-023-01022-4
18.	W. Ouyang, W. Lu, Y. Zhang, Y. Liu, J.U. Kim et al., A wireless and battery-less implant for multimodal closed-loop neuromodulation in small animals. Nat. Biomed. Eng. 7, 1252-1269 (2023). https://doi.org/10.1038/s41551-023-01029-x
19.	J. Tu, J. Min, Y. Song, C. Xu, J. Li et al., A wireless patch for the monitoring of C-reactive protein in sweat. Nat. Biomed. Eng. 7, 1293-1306 (2023). https://doi.org/10.1038/s41551-023-01059-5
20.	S. Kim, Y.S. Oh, K. Lee, S. Kim, W.-Y. Maeng et al., Battery-free, wireless, cuff-type, multimodal physical sensor for continuous temperature and strain monitoring of nerve. Small 19, 2206839 (2023). https://doi.org/10.1002/smll.202206839
21.	R. Chen, T. Luo, D. Geng, Z. Shen, W. Zhou, Facile fabrication of a fast-response flexible temperature sensor via laser reduced graphene oxide for contactless human-machine interface. Carbon 187, 35-46 (2022). https://doi.org/10.1016/j.carbon.2021.10.064
22.	C. Okutani, T. Yokota, T. Someya, Ultrathin fiber-mesh polymer thermistors. Adv. Sci. 9, e2202312 (2022). https://doi.org/10.1002/advs.202202312
23.	C. Okutani, T. Yokota, R. Matsukawa, T. Someya, Suppressing the negative temperature coefficient effect of resistance in polymer composites with positive temperature coefficients of resistance by coating with parylene. J. Mater. Chem. C 8, 7304-7308 (2020). https://doi.org/10.1039/D0TC00702A
24.	M. Sang, K. Kang, Y. Zhang, H. Zhang, K. Kim et al., Ultrahigh sensitive Au-doped silicon nanomembrane based wearable sensor arrays for continuous skin temperature monitoring with high precision. Adv. Mater. 34, e2105865 (2022). https://doi.org/10.1002/adma.202105865
25.	G.Y. Bae, J.T. Han, G. Lee, S. Lee, S.W. Kim et al., Pressure/temperature sensing bimodal electronic skin with stimulus discriminability and linear sensitivity. Adv. Mater. 30, e1803388 (2018). https://doi.org/10.1002/adma.201803388
26.	M. Li, Y. Shi, H. Gao, Z. Chen, Bio-inspired nanospiky metal particles enable thin, flexible, and thermo-responsive polymer nanocomposites for thermal regulation. Adv. Funct. Mater. 30, 1910328 (2020). https://doi.org/10.1002/adfm.201910328
27.	M. Li, G. Cai, J. Holoubek, K. Yu, H. Liu et al., Hierarchically structured metal carbides as conductive fillers in thermo-responsive polymer nanocomposites for battery safety. Nano Energy 103, 107726 (2022). https://doi.org/10.1016/j.nanoen.2022.107726
28.	Z. Chen, P.-C. Hsu, J. Lopez, Y. Li, J.W.F. To et al., Fast and reversible thermoresponsive polymer switching materials for safer batteries. Nat. Energy 1, 15009 (2016). https://doi.org/10.1038/nenergy.2015.9
29.	T. Yokota, Y. Inoue, Y. Terakawa, J. Reeder, M. Kaltenbrunner et al., Ultraflexible, large-area, physiological temperature sensors for multipoint measurements. Proc. Natl. Acad. Sci. U.S.A. 112, 14533-14538 (2015). https://doi.org/10.1073/pnas.1515650112
30.	M. Li, K. Chang, W. Zhong, C. Xiang, W. Wang et al., A highly stretchable, breathable and thermoregulatory electronic skin based on the polyolefin elastomer nanofiber membrane. Appl. Surf. Sci. 486, 249-256 (2019). https://doi.org/10.1016/j.apsusc.2019.04.271
31.	S. Xiang, D. Liu, C. Jiang, W. Zhou, D. Ling et al., Liquid-metal-based dynamic thermoregulating and self-powered electronic skin. Adv. Funct. Mater. 31, 2100940 (2021). https://doi.org/10.1002/adfm.202100940
32.	S. Xiang, J. Tang, L. Yang, Y. Guo, Z. Zhao et al., Deep learning-enabled real-time personal handwriting electronic skin with dynamic thermoregulating ability. npj Flex. Electron. 6, 59 (2022). https://doi.org/10.1038/s41528-022-00195-3
33.	J. Huang, Z. Xu, W. Qiu, F. Chen, Z. Meng et al., Stretchable and heat-resistant protein-based electronic skin for human thermoregulation. Adv. Funct. Mater. 30, 1910547 (2020). https://doi.org/10.1002/adfm.201910547
34.	J. Wu, W. Huang, Y. Liang, Z. Wu, B. Zhong et al., Self-calibrated, sensitive, and flexible temperature sensor based on 3D chemically modified graphene hydrogel. Adv. Electron. Mater. 7, 2001084 (2021). https://doi.org/10.1002/aelm.202001084
35.	R. You, Y.-Q. Liu, Y.-L. Hao, D.-D. Han, Y.-L. Zhang et al., Laser fabrication of graphene-based flexible electronics. Adv. Mater. 32, 1901981 (2020). https://doi.org/10.1002/adma.201901981
36.	T.S.D. Le, H.P. Phan, S. Kwon, S. Park, Y. Jung et al., Recent advances in laser-induced graphene: mechanism, fabrication, properties, and applications in flexible electronics. Adv. Funct. Mater. 32, 2205158 (2022). https://doi.org/10.1002/adfm.202205158
37.	G. Karimi, I. Lau, M. Fowler, M. Pope, Parametric study of laser-induced graphene conductive traces and their application as flexible heaters. Int. J. Energy Res. 45, 13712-13725 (2021). https://doi.org/10.1002/er.6701
38.	Z. Sun, S. Fang, Y.H. Hu, 3D graphene materials: from understanding to design and synthesis control. Chem. Rev. 120, 10336-10453 (2020). https://doi.org/10.1021/acs.chemrev.0c00083
39.	J. Xu, R. Li, S. Ji, B. Zhao, T. Cui et al., Multifunctional graphene microstructures inspired by honeycomb for ultrahigh performance electromagnetic interference shielding and wearable applications. ACS Nano 15, 8907-8918 (2021). https://doi.org/10.1021/acsnano.1c01552
40.	Y. Qiao, Y. Wang, H. Tian, M. Li, J. Jian et al., Multilayer graphene epidermal electronic skin. ACS Nano 12, 8839-8846 (2018). https://doi.org/10.1021/acsnano.8b02162
41.	S.Y. Xia, Y. Long, Z. Huang, Y. Zi, L.Q. Tao et al., Laser-induced graphene (LIG)-based pressure sensor and triboelectric nanogenerator toward high-performance self-powered measurement-control combined system. Nano Energy 96, 107099 (2022). https://doi.org/10.1016/j.nanoen.2022.107099
42.	J. Jeon, H.-B.-R. Lee, Z. Bao, Flexible wireless temperature sensors based on Ni microparticle-filled binary polymer composites. Adv. Mater. 25, 850-855 (2013). https://doi.org/10.1002/adma.201204082
43.	Y. Geng, R. Cao, M.T. Innocent, Z. Hu, L. Zhu et al., A high-sensitive wearable sensor based on conductive polymer composites for body temperature monitoring. Compos. Part A Appl. Sci. Manuf. 163, 107269 (2022). https://doi.org/10.1016/j.compositesa.2022.107269
44.	L. Liu, R. Li, F. Liu, L. Huang, W. Liu et al., Highly elastic and strain sensing corn protein electrospun fibers for monitoring of wound healing. ACS Nano 17, 9600-9610 (2023). https://doi.org/10.1021/acsnano.3c03087
45.	X. Tang, X. Chen, S. Zhang, X. Gu, R. Wu et al., Silk-inspired in situ hydrogel with anti-tumor immunity enhanced photodynamic therapy for melanoma and infected wound healing. Adv. Funct. Mater. 31, 2101320 (2021). https://doi.org/10.1002/adfm.202101320
46.	X. Xu, X. Liu, L. Tan, Z. Cui, X. Yang et al., Controlled-temperature photothermal and oxidative bacteria killing and acceleration of wound healing by polydopamine-assisted Au-hydroxyapatite nanorods. Acta Biomater. 77, 352-364 (2018). https://doi.org/10.1016/j.actbio.2018.07.030
47.	T. Someya, Z. Bao, G.G. Malliaras, The Rise of plastic bioelectronics. Nature 540, 379-385 (2016). https://doi.org/10.1038/nature21004

[1]	CHEN Lu (陈露), CHENG Liying (程丽英), CHEN Tian (陈田), ZHANG Yuguang (张余光), ZHANG Jianming* (张建明). Macrophage Polarization in Skin Wound Healing: Progress in Biology and Therapeutics [J]. J Shanghai Jiaotong Univ Sci, 2022, 27(2): 264-280.
[2]	CAI Weijie (蔡伟杰), HAMUSHAN Musha (木沙·哈木山), ZHAO Changli (赵常利), CHENG Pengfei (程鹏飞), ZHONG Wanrun (钟万润), HAN Pei (韩培). Influence of Supramolecular Chiral Hydrogel on Cellular Behavior of Endothelial Cells Under High-Glucose-Induced Injury [J]. J Shanghai Jiaotong Univ Sci, 2021, 26(1): 17-24.
[3]	Xi Zhou, Quan Zhou, Zhaozhi He, Yi Xiao, Yan Liu, Zhuohang Huang, Yaoji Sun, Jiawei Wang, Zhengdong Zhao, Xiaozhou Liu, Bin Zhou, Lei Ren, Yu Sun, Zhiwei Chen, Xingcai Zhang. ROS Balance Autoregulating Core-Shell CeO₂@ZIF-8/Au Nanoplatform for Wound Repair [J]. Nano-Micro Letters, 2024, 16(1): 156-.

Please choose a citation manager

Content to export