Gelatin-Based Metamaterial Hydrogel Films with High Conformality for Ultra-Soft Tissue Monitoring
Corresponding Author: Yong He
Nano-Micro Letters,
Vol. 16 (2024), Article Number: 34
Abstract
Implantable hydrogel-based bioelectronics (IHB) can precisely monitor human health and diagnose diseases. However, achieving biodegradability, biocompatibility, and high conformality with soft tissues poses significant challenges for IHB. Gelatin is the most suitable candidate for IHB since it is a collagen hydrolysate and a substantial part of the extracellular matrix found naturally in most tissues. This study used 3D printing ultrafine fiber networks with metamaterial design to embed into ultra-low elastic modulus hydrogel to create a novel gelatin-based conductive film (GCF) with mechanical programmability. The regulation of GCF nearly covers soft tissue mechanics, an elastic modulus from 20 to 420 kPa, and a Poisson's ratio from − 0.25 to 0.52. The negative Poisson's ratio promotes conformality with soft tissues to improve the efficiency of biological interfaces. The GCF can monitor heartbeat signals and respiratory rate by determining cardiac deformation due to its high conformability. Notably, the gelatin characteristics of the biodegradable GCF enable the sensor to monitor and support tissue restoration. The GCF metamaterial design offers a unique idea for bioelectronics to develop implantable sensors that integrate monitoring and tissue repair and a customized method for endowing implanted sensors to be highly conformal with soft tissues.
Highlights:
1 Novel customized metamaterial gelatin-based conductive film (GCF) was developed to ensure good biocompatibility and biodegradability for implantable bioelectronics integrating monitoring with tissue repair. The metamaterial property demonstrated high conformal with soft tissues to promote the signal-to-noise ratio.
2 The GCF revealed elastic modulus regulated from 20 to 420 kPa and Poisson's ratio from − 0.25 to 0.52. It was fabricated by embedding different 3D printing ultrafine fiber networks with metamaterial design into ultra-low modulus Gelatin methacryloyl hydrogel.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- Y. Min, R. Han, G. Li, X. Wang, S. Chen et al., The pH-sensitive optical fiber integrated CMCS-PA@Fe hydrogels for photothermal therapy and real-time monitoring of infected wounds. Adv. Funct. Mater. (2023). https://doi.org/10.1002/adfm.202212803
- Y. Jiang, A.A. Trotsyuk, S. Niu, D. Henn, K. Chen et al., Wireless, closed-loop, smart bandage with integrated sensors and stimulators for advanced wound care and accelerated healing. Nat. Biotechnol. (2022). https://doi.org/10.1038/s41587-022-01528-3
- Q. Liang, X. Xia, X. Sun, D. Yu, X. Huang et al., Highly stretchable hydrogels as wearable and implantable sensors for recording physiological and brain neural signals. Adv. Sci. 9(16), 2201059 (2022). https://doi.org/10.1002/advs.202201059
- Q. Liang, Z. Shen, X. Sun, D. Yu, K. Liu et al., Electron conductive and transparent hydrogels for recording brain neural signals and neuromodulation. Adv. Mater. 35(9), 2211159 (2023). https://doi.org/10.1002/adma.202211159
- G. Li, K. Huang, J. Deng, M. Guo, M. Cai et al., Highly conducting and stretchable double-network hydrogel for soft bioelectronics. Adv. Mater. 34(15) (2022). https://doi.org/10.1002/adma.202200261
- K. Sim, F. Ershad, Y. Zhang, P. Yang, H. Shim et al., An epicardial bioelectronic patch made from soft rubbery materials and capable of spatiotemporal mapping of electrophysiological activity. Nat. Electron. 3(12), 775–784 (2020). https://doi.org/10.1038/s41928-020-00493-6
- J. Zhang, S. Shen, R. Lin, J. Huang, C. Pu et al., Highly stretchable and biocompatible wrinkled nanoclay-composite hydrogel with enhanced sensing capability for precise detection of myocardial infarction. Adv. Mater. 35(9), 2209497 (2023). https://doi.org/10.1002/adma.202209497
- S. Wang, Y. Nie, H. Zhu, Y. Xu, S. Cao et al., Intrinsically stretchable electronics with ultrahigh deformability to monitor dynamically moving organs. Sci. Adv. 8(13), l5511 (2022). https://doi.org/10.1126/sciadv.abl5511
- P. Wu, Z. Wang, X. Yao, J. Fu, Y. He, Recyclable conductive nanoclay for direct in situ printing flexible electronics. Mater. Horiz. 8(7), 2006–2017 (2021). https://doi.org/10.1039/d0mh02065f
- Z. Wang, C. Luan, G. Liao, J. Liu, X. Yao, J. Fu, High-performance auxetic bilayer conductive mesh-based multi-material integrated stretchable strain sensors. ACS Appl. Mater. Inter. 13(19), 23038–23048 (2021). https://doi.org/10.1021/acsami.1c06295
- Y. Wan, Z. Qiu, Y. Hong, Y. Wang, J. Zhang et al., A highly sensitive flexible capacitive tactile sensor with sparse and high-aspect-ratio microstructures. Adv. Electron. Mater. 4(4), 1700586 (2018). https://doi.org/10.1002/aelm.201700586
- Y. Chen, H. Yang, Octopus-inspired assembly of nanosucker arrays for dry/wet adhesion. ACS Nano 11(6), 5332–5338 (2017). https://doi.org/10.1021/acsnano.7b00809
- M.B. Christensen, S.M. Pearce, N.M. Ledbetter, D.J. Warren, G.A. Clark et al., The foreign body response to the utah slant electrode array in the cat sciatic nerve. Acta Biomater. 10(11), 4650–4660 (2014). https://doi.org/10.1016/j.actbio.2014.07.010
- J.H. Lee, S.H. Kim, J.S. Heo, J.Y. Kwak, C.W. Park et al., Heterogeneous structure omnidirectional strain sensor arrays with cognitively learned neural networks. Adv. Mater. (2023). https://doi.org/10.1002/adma.202208184
- J. Shi, Y. Dai, Y. Cheng, S. Xie, G. Li et al., Embedment of sensing elements for robust, highly sensitive, and cross-talk-free iontronic skins for robotics applications. Sci. Adv. 9(9), f8831 (2023). https://doi.org/10.1126/sciadv.adf8831
- S. Liu, Y. Rao, H. Jang, P. Tan, N. Lu, Strategies for body-conformable electronics. Matter 5(4), 1104–1136 (2022). https://doi.org/10.1016/j.matt.2022.02.006
- Y. Ma, X. Feng, J.A. Rogers, Y. Huang, Y. Zhang, Design and application of “J-shaped” stress-strain behavior in stretchable electronics: a review. Lab Chip 17(1), 1174–1689 (2017). https://doi.org/10.1039/c7lc00289k
- X. Li, L. He, Y. Li, M. Chao, M. Li et al., Healable, degradable, and conductive MXene nanocomposite hydrogel for multifunctional epidermal sensors. ACS Nano 15(4), 7765–7773 (2021). https://doi.org/10.1021/acsnano.1c01751
- Z.S.G.A. Khatri, Matrix metalloproteinases in vascular remodeling and atherogenesis. Circ. Res. 90(3), 251–262 (2002). https://doi.org/10.1161/hh0302.105345
- P.D.B.N. Van den Steen, Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. 37, 375–536 (2002). https://doi.org/10.1080/10409230290771546
- U. Hersel, C. Dahmen, H. Kessler, RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24(24), 4385–4415 (2003). https://doi.org/10.1016/S0142-9612(03)00343-0
- P. Schaffner, M.M. Dard, Structure and function of RGD peptides involved in bone biology. Cell. Mol. Life Sci. 60(1), 119–132 (2003). https://doi.org/10.1007/s000180300008
- S.L. Bellis, Advantages of RGD peptides for directing cell association with biomaterials. Biomaterials 32(18), 4205–4210 (2011). https://doi.org/10.1016/j.biomaterials.2011.02.029
- M.C. Gómez-Guillén, B. Giménez, M.E. López-Caballero, M.P. Montero, Functional and bioactive properties of collagen and gelatin from alternative sources: a review. Food Hydrocoll. 25(8), 1813–1827 (2011). https://doi.org/10.1016/j.foodhyd.2011.02.007
- A.G. Kurian, R.K. Singh, K.D. Patel, J. Lee, H. Kim, Multifunctional GelMA platforms with nanomaterials for advanced tissue therapeutics. Bioact. Mater. 8, 267–295 (2022). https://doi.org/10.1016/j.bioactmat.2021.06.027
- K. Yue, G. Trujillo-De Santiago, M.M. Alvarez, A. Tamayol, N. Annabi, A. Khademhosseini, Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 73, 254–271 (2015). https://doi.org/10.1016/j.biomaterials.2015.08.045
- X. Wang, Z. Bai, M. Zheng, O. Yue, M. Hou et al., Engineered gelatin-based conductive hydrogels for flexible wearable electronic devices: fundamentals and recent advances. J. Sci-Adv. Mater. Dev. 7(3), 100451 (2022). https://doi.org/10.1016/j.jsamd.2022.100451
- G. Kavoosi, Z. Bordbar, S.M. Dadfar, S.M.M. Dadfar, Preparation and characterization of a novel gelatin-poly (vinyl alcohol) hydrogel film loaded with Zataria multiflora essential oil for antibacterial-antioxidant wound-dressing applications. J. Appl. Polym. Sci. 134(39), 45351 (2017). https://doi.org/10.1002/app.45351
- X. Zhang, T. Ye, X. Meng, Z. Tian, L. Pang et al., Sustainable and transparent fish gelatin films for flexible electroluminescent devices. ACS Nano 14(4), 3876–3884 (2020). https://doi.org/10.1021/acsnano.9b09880
- G.C.S.P.A. Bigi, Mechanical and thermal properties of gelatin films at different degrees of glutaraldehyde crosslinking. Biomaterials 2001(22), 763–768 (2001). https://doi.org/10.1016/S0142-9612(00)00236-2
- J. Visser, F.P.W. Melchels, J.E. Jeon, E.M. van Bussel, L.S. Kimpton et al., Reinforcement of hydrogels using three-dimensionally printed microfibres. Nat. Commun. 6(1), 7933 (2015). https://doi.org/10.1038/ncomms7933
- O. Bas, E.M. De-Juan-Pardo, M.P. Chhaya, F.M. Wunner, J.E. Jeon et al., Enhancing structural integrity of hydrogels by using highly organised melt electrospun fibre constructs. Eur. Polym. J. 72, 451–463 (2015). https://doi.org/10.1016/j.eurpolymj.2015.07.034
- O. Bas, D.D. Angella, J.G. Baldwin, N.J. Castro, F.M. Wunner et al., An integrated design, material, and fabrication platform for engineering biomechanically and biologically functional soft tissues. ACS Appl. Mater. Inter. 9(35), 29430–29437 (2017). https://doi.org/10.1021/acsami.7b08617
- T.M. Robinson, D.W. Hutmacher, P.D. Dalton, The next frontier in melt electrospinning: taming the jet. Adv. Funct. Mater. 29(44), 1904664 (2019). https://doi.org/10.1002/adfm.201904664
- S. Lv, J. Nie, Q. Gao, C. Xie, L. Zhou et al., Micro/nanofabrication of brittle hydrogels using 3D printed soft ultrafine fiber molds for damage-free demolding. Biofabrication 12(2), 25015 (2020). https://doi.org/10.1088/1758-5090/ab57d8
- C. Xie, Q. Gao, P. Wang, L. Shao, H. Yuan et al., Structure-induced cell growth by 3D printing of heterogeneous scaffolds with ultrafine fibers. Mater. Design 181, 108092 (2019). https://doi.org/10.1016/j.matdes.2019.108092
- Q. Gao, C. Xie, P. Wang, M. Xie, H. Li et al., 3D printed multi-scale scaffolds with ultrafine fibers for providing excellent biocompatibility. Mater. Sci. Eng. C 107, 110269 (2020). https://doi.org/10.1016/j.msec.2019.110269
- Y. Li, S. Lv, H. Yuan, G. Ye, W. Mu et al., Peripheral nerve regeneration with 3D printed bionic scaffolds loading neural crest stem cell derived schwann cell progenitors. Adv. Funct. Mater. 31(16), 2010215 (2021). https://doi.org/10.1002/adfm.202010215
- S. Jiang, X. Liu, J. Liu, D. Ye, Y. Duan et al., Flexible metamaterial electronics. Adv. Mater. 34(52), 2200070 (2022). https://doi.org/10.1002/adma.202200070
- J. He, Y. Sun, Q. Gao, C. He, K. Yao et al., Gelatin methacryloyl hydrogel, from standardization, performance, to biomedical application. Adv. Healthc. Mater. (2023). https://doi.org/10.1002/adhm.202300395
- X. Yao, S. Zhang, L. Qian, N. Wei, V. Nica et al., Super stretchable, self-healing, adhesive ionic conductive hydrogels based on tailor-made ionic liquid for high-performance strain sensors. Adv. Funct. Mater. 32(33), 2204565 (2022). https://doi.org/10.1002/adfm.202204565
- K. Min Seong, L. Yung, A. Junseong, K. Seonggi, K. Kyungnam et al., Skin-like omnidirectional stretchable platform with negative Poisson’s ratio for wearable strain–pressure simultaneous sensor. Adv. Funct. Mater. (2022). https://doi.org/10.1002/adfm.202208792
- H. Liu, Y. Li, M. Zhou, B. Chen, Y. Chen et al., Ambilateral convergent directional freeze casting meta-structured foams with a negative Poisson’s ratio for high-performance piezoresistive sensors. Chem. Eng. J. 454, 140436 (2023). https://doi.org/10.1016/j.cej.2022.140436
- S.K. Kundu, S. Kumagai, M. Sasaki, A wearable capacitive sensor for monitoring human respiratory rate. JPN. J. Appl. Phys. 52(4), 4C-5C (2013). https://doi.org/10.7567/JJAP.52.04CL05
- H. Kawaoka, T. Yamada, M. Matsushima, T. Kawabe, Y. Hasegawa et al., Heartbeat signal detection from analysis of airflow in rat airway under different depths of anaesthesia conditions. IEEE Sens. J. 17(14), 4369–4377 (2017). https://doi.org/10.1109/JSEN.2017.2707594
- E. Bouairi, R. Neff, C. Evans, A. Gold, M.C. Andresen et al., Respiratory sinus arrhythmia in freely moving and anesthetized rats. J. Appl. Physiol. 97(4), 1431–1436 (2004). https://doi.org/10.1152/japplphysiol.00277.2004
References
Y. Min, R. Han, G. Li, X. Wang, S. Chen et al., The pH-sensitive optical fiber integrated CMCS-PA@Fe hydrogels for photothermal therapy and real-time monitoring of infected wounds. Adv. Funct. Mater. (2023). https://doi.org/10.1002/adfm.202212803
Y. Jiang, A.A. Trotsyuk, S. Niu, D. Henn, K. Chen et al., Wireless, closed-loop, smart bandage with integrated sensors and stimulators for advanced wound care and accelerated healing. Nat. Biotechnol. (2022). https://doi.org/10.1038/s41587-022-01528-3
Q. Liang, X. Xia, X. Sun, D. Yu, X. Huang et al., Highly stretchable hydrogels as wearable and implantable sensors for recording physiological and brain neural signals. Adv. Sci. 9(16), 2201059 (2022). https://doi.org/10.1002/advs.202201059
Q. Liang, Z. Shen, X. Sun, D. Yu, K. Liu et al., Electron conductive and transparent hydrogels for recording brain neural signals and neuromodulation. Adv. Mater. 35(9), 2211159 (2023). https://doi.org/10.1002/adma.202211159
G. Li, K. Huang, J. Deng, M. Guo, M. Cai et al., Highly conducting and stretchable double-network hydrogel for soft bioelectronics. Adv. Mater. 34(15) (2022). https://doi.org/10.1002/adma.202200261
K. Sim, F. Ershad, Y. Zhang, P. Yang, H. Shim et al., An epicardial bioelectronic patch made from soft rubbery materials and capable of spatiotemporal mapping of electrophysiological activity. Nat. Electron. 3(12), 775–784 (2020). https://doi.org/10.1038/s41928-020-00493-6
J. Zhang, S. Shen, R. Lin, J. Huang, C. Pu et al., Highly stretchable and biocompatible wrinkled nanoclay-composite hydrogel with enhanced sensing capability for precise detection of myocardial infarction. Adv. Mater. 35(9), 2209497 (2023). https://doi.org/10.1002/adma.202209497
S. Wang, Y. Nie, H. Zhu, Y. Xu, S. Cao et al., Intrinsically stretchable electronics with ultrahigh deformability to monitor dynamically moving organs. Sci. Adv. 8(13), l5511 (2022). https://doi.org/10.1126/sciadv.abl5511
P. Wu, Z. Wang, X. Yao, J. Fu, Y. He, Recyclable conductive nanoclay for direct in situ printing flexible electronics. Mater. Horiz. 8(7), 2006–2017 (2021). https://doi.org/10.1039/d0mh02065f
Z. Wang, C. Luan, G. Liao, J. Liu, X. Yao, J. Fu, High-performance auxetic bilayer conductive mesh-based multi-material integrated stretchable strain sensors. ACS Appl. Mater. Inter. 13(19), 23038–23048 (2021). https://doi.org/10.1021/acsami.1c06295
Y. Wan, Z. Qiu, Y. Hong, Y. Wang, J. Zhang et al., A highly sensitive flexible capacitive tactile sensor with sparse and high-aspect-ratio microstructures. Adv. Electron. Mater. 4(4), 1700586 (2018). https://doi.org/10.1002/aelm.201700586
Y. Chen, H. Yang, Octopus-inspired assembly of nanosucker arrays for dry/wet adhesion. ACS Nano 11(6), 5332–5338 (2017). https://doi.org/10.1021/acsnano.7b00809
M.B. Christensen, S.M. Pearce, N.M. Ledbetter, D.J. Warren, G.A. Clark et al., The foreign body response to the utah slant electrode array in the cat sciatic nerve. Acta Biomater. 10(11), 4650–4660 (2014). https://doi.org/10.1016/j.actbio.2014.07.010
J.H. Lee, S.H. Kim, J.S. Heo, J.Y. Kwak, C.W. Park et al., Heterogeneous structure omnidirectional strain sensor arrays with cognitively learned neural networks. Adv. Mater. (2023). https://doi.org/10.1002/adma.202208184
J. Shi, Y. Dai, Y. Cheng, S. Xie, G. Li et al., Embedment of sensing elements for robust, highly sensitive, and cross-talk-free iontronic skins for robotics applications. Sci. Adv. 9(9), f8831 (2023). https://doi.org/10.1126/sciadv.adf8831
S. Liu, Y. Rao, H. Jang, P. Tan, N. Lu, Strategies for body-conformable electronics. Matter 5(4), 1104–1136 (2022). https://doi.org/10.1016/j.matt.2022.02.006
Y. Ma, X. Feng, J.A. Rogers, Y. Huang, Y. Zhang, Design and application of “J-shaped” stress-strain behavior in stretchable electronics: a review. Lab Chip 17(1), 1174–1689 (2017). https://doi.org/10.1039/c7lc00289k
X. Li, L. He, Y. Li, M. Chao, M. Li et al., Healable, degradable, and conductive MXene nanocomposite hydrogel for multifunctional epidermal sensors. ACS Nano 15(4), 7765–7773 (2021). https://doi.org/10.1021/acsnano.1c01751
Z.S.G.A. Khatri, Matrix metalloproteinases in vascular remodeling and atherogenesis. Circ. Res. 90(3), 251–262 (2002). https://doi.org/10.1161/hh0302.105345
P.D.B.N. Van den Steen, Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit. Rev. Biochem. Mol. 37, 375–536 (2002). https://doi.org/10.1080/10409230290771546
U. Hersel, C. Dahmen, H. Kessler, RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 24(24), 4385–4415 (2003). https://doi.org/10.1016/S0142-9612(03)00343-0
P. Schaffner, M.M. Dard, Structure and function of RGD peptides involved in bone biology. Cell. Mol. Life Sci. 60(1), 119–132 (2003). https://doi.org/10.1007/s000180300008
S.L. Bellis, Advantages of RGD peptides for directing cell association with biomaterials. Biomaterials 32(18), 4205–4210 (2011). https://doi.org/10.1016/j.biomaterials.2011.02.029
M.C. Gómez-Guillén, B. Giménez, M.E. López-Caballero, M.P. Montero, Functional and bioactive properties of collagen and gelatin from alternative sources: a review. Food Hydrocoll. 25(8), 1813–1827 (2011). https://doi.org/10.1016/j.foodhyd.2011.02.007
A.G. Kurian, R.K. Singh, K.D. Patel, J. Lee, H. Kim, Multifunctional GelMA platforms with nanomaterials for advanced tissue therapeutics. Bioact. Mater. 8, 267–295 (2022). https://doi.org/10.1016/j.bioactmat.2021.06.027
K. Yue, G. Trujillo-De Santiago, M.M. Alvarez, A. Tamayol, N. Annabi, A. Khademhosseini, Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials 73, 254–271 (2015). https://doi.org/10.1016/j.biomaterials.2015.08.045
X. Wang, Z. Bai, M. Zheng, O. Yue, M. Hou et al., Engineered gelatin-based conductive hydrogels for flexible wearable electronic devices: fundamentals and recent advances. J. Sci-Adv. Mater. Dev. 7(3), 100451 (2022). https://doi.org/10.1016/j.jsamd.2022.100451
G. Kavoosi, Z. Bordbar, S.M. Dadfar, S.M.M. Dadfar, Preparation and characterization of a novel gelatin-poly (vinyl alcohol) hydrogel film loaded with Zataria multiflora essential oil for antibacterial-antioxidant wound-dressing applications. J. Appl. Polym. Sci. 134(39), 45351 (2017). https://doi.org/10.1002/app.45351
X. Zhang, T. Ye, X. Meng, Z. Tian, L. Pang et al., Sustainable and transparent fish gelatin films for flexible electroluminescent devices. ACS Nano 14(4), 3876–3884 (2020). https://doi.org/10.1021/acsnano.9b09880
G.C.S.P.A. Bigi, Mechanical and thermal properties of gelatin films at different degrees of glutaraldehyde crosslinking. Biomaterials 2001(22), 763–768 (2001). https://doi.org/10.1016/S0142-9612(00)00236-2
J. Visser, F.P.W. Melchels, J.E. Jeon, E.M. van Bussel, L.S. Kimpton et al., Reinforcement of hydrogels using three-dimensionally printed microfibres. Nat. Commun. 6(1), 7933 (2015). https://doi.org/10.1038/ncomms7933
O. Bas, E.M. De-Juan-Pardo, M.P. Chhaya, F.M. Wunner, J.E. Jeon et al., Enhancing structural integrity of hydrogels by using highly organised melt electrospun fibre constructs. Eur. Polym. J. 72, 451–463 (2015). https://doi.org/10.1016/j.eurpolymj.2015.07.034
O. Bas, D.D. Angella, J.G. Baldwin, N.J. Castro, F.M. Wunner et al., An integrated design, material, and fabrication platform for engineering biomechanically and biologically functional soft tissues. ACS Appl. Mater. Inter. 9(35), 29430–29437 (2017). https://doi.org/10.1021/acsami.7b08617
T.M. Robinson, D.W. Hutmacher, P.D. Dalton, The next frontier in melt electrospinning: taming the jet. Adv. Funct. Mater. 29(44), 1904664 (2019). https://doi.org/10.1002/adfm.201904664
S. Lv, J. Nie, Q. Gao, C. Xie, L. Zhou et al., Micro/nanofabrication of brittle hydrogels using 3D printed soft ultrafine fiber molds for damage-free demolding. Biofabrication 12(2), 25015 (2020). https://doi.org/10.1088/1758-5090/ab57d8
C. Xie, Q. Gao, P. Wang, L. Shao, H. Yuan et al., Structure-induced cell growth by 3D printing of heterogeneous scaffolds with ultrafine fibers. Mater. Design 181, 108092 (2019). https://doi.org/10.1016/j.matdes.2019.108092
Q. Gao, C. Xie, P. Wang, M. Xie, H. Li et al., 3D printed multi-scale scaffolds with ultrafine fibers for providing excellent biocompatibility. Mater. Sci. Eng. C 107, 110269 (2020). https://doi.org/10.1016/j.msec.2019.110269
Y. Li, S. Lv, H. Yuan, G. Ye, W. Mu et al., Peripheral nerve regeneration with 3D printed bionic scaffolds loading neural crest stem cell derived schwann cell progenitors. Adv. Funct. Mater. 31(16), 2010215 (2021). https://doi.org/10.1002/adfm.202010215
S. Jiang, X. Liu, J. Liu, D. Ye, Y. Duan et al., Flexible metamaterial electronics. Adv. Mater. 34(52), 2200070 (2022). https://doi.org/10.1002/adma.202200070
J. He, Y. Sun, Q. Gao, C. He, K. Yao et al., Gelatin methacryloyl hydrogel, from standardization, performance, to biomedical application. Adv. Healthc. Mater. (2023). https://doi.org/10.1002/adhm.202300395
X. Yao, S. Zhang, L. Qian, N. Wei, V. Nica et al., Super stretchable, self-healing, adhesive ionic conductive hydrogels based on tailor-made ionic liquid for high-performance strain sensors. Adv. Funct. Mater. 32(33), 2204565 (2022). https://doi.org/10.1002/adfm.202204565
K. Min Seong, L. Yung, A. Junseong, K. Seonggi, K. Kyungnam et al., Skin-like omnidirectional stretchable platform with negative Poisson’s ratio for wearable strain–pressure simultaneous sensor. Adv. Funct. Mater. (2022). https://doi.org/10.1002/adfm.202208792
H. Liu, Y. Li, M. Zhou, B. Chen, Y. Chen et al., Ambilateral convergent directional freeze casting meta-structured foams with a negative Poisson’s ratio for high-performance piezoresistive sensors. Chem. Eng. J. 454, 140436 (2023). https://doi.org/10.1016/j.cej.2022.140436
S.K. Kundu, S. Kumagai, M. Sasaki, A wearable capacitive sensor for monitoring human respiratory rate. JPN. J. Appl. Phys. 52(4), 4C-5C (2013). https://doi.org/10.7567/JJAP.52.04CL05
H. Kawaoka, T. Yamada, M. Matsushima, T. Kawabe, Y. Hasegawa et al., Heartbeat signal detection from analysis of airflow in rat airway under different depths of anaesthesia conditions. IEEE Sens. J. 17(14), 4369–4377 (2017). https://doi.org/10.1109/JSEN.2017.2707594
E. Bouairi, R. Neff, C. Evans, A. Gold, M.C. Andresen et al., Respiratory sinus arrhythmia in freely moving and anesthetized rats. J. Appl. Physiol. 97(4), 1431–1436 (2004). https://doi.org/10.1152/japplphysiol.00277.2004