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  • Review Article
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Tissue–electronics interfaces: from implantable devices to engineered tissues

Nature Reviews Materials volume 3, Article number: 17076 (2018) Cite this article

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Abstract

Biomedical electronic devices are interfaced with the human body to extract precise medical data and to interfere with tissue function by providing electrical stimuli. In this Review, we outline physiologically and pathologically relevant tissue properties and processes that are important for designing implantable electronic devices. We summarize design principles for flexible and stretchable electronics that adapt to the mechanics of soft tissues, such as those including conducting polymers, liquid metal alloys, metallic buckling and meandering architectures. We further discuss technologies for inserting devices into the body in a minimally invasive manner and for eliminating them without further intervention. Finally, we introduce the concept of integrating electronic devices with biomaterials and cells, and we envision how such technologies may lead to the development of bionic organs for regenerative medicine.

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Figure 1: Timeline of implantable electronic devices.
Figure 2: Tissue and organ properties important for biomedical implants.
Figure 3: Fabrication principles of stretchable electronics.
Figure 4: Transient electronics.
Figure 5: Minimally invasive electronics.

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References

  1. Aquilina, O. A brief history of cardiac pacing. Images Paediatr. Cardiol. 27, 17–81 (2006).

    Google Scholar 

  2. Morton, P. G. Rate-responsive cardiac pacemakers. AACN Adv. Crit. Care 2, 140–149 (1991).

    Article  CAS  Google Scholar 

  3. Tomaske, M. et al. A 12-year experience of bipolar steroid-eluting epicardial pacing leads in children. Ann. Thorac. Surg. 85, 1694–1701 (2008).

    Article  Google Scholar 

  4. Cohen, M. I. et al. Permanent epicardial pacing in pediatric patients. Circulation 103, 2585–2590 (2001).

    Article  CAS  Google Scholar 

  5. Zeng, F.-G. & Fay, R. R. Cochlear Implants: Auditory Prostheses and Electric Hearing 1–13 (Springer, 2004).

    Google Scholar 

  6. Zeng, F.-G. & Fay, R. R. Cochlear Implants: Auditory prostheses and Electric Hearing (Springer, 2013).

    Google Scholar 

  7. Wilson, B. S. & Dorman, M. F. Cochlear implants: current designs and future possibilities. J. Rehabil. Res. Dev. 45, 695 (2008).

    Article  Google Scholar 

  8. Lacour, S. P., Courtine, G. & Guck, J. Materials and technologies for soft implantable neuroprostheses. Nat. Rev. Mater. 1, 15963 (2016).

    Article  CAS  Google Scholar 

  9. Fleischer, S. & Dvir, T. Tissue engineering on the nanoscale: lessons from the heart. Curr. Opin. Biotechnol. 24, 664–671 (2013).

    Article  CAS  Google Scholar 

  10. Allen, D. & Kurihara, S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J. Physiol. 327, 79 (1982).

    Article  CAS  Google Scholar 

  11. Carlsson, M. et al. Total heart volume variation throughout the cardiac cycle in humans. Am. J. Physiol. Heart Circ. Physiol. 287, H243–H250 (2004).

    Article  CAS  Google Scholar 

  12. Close, R. Dynamic properties of mammalian skeletal muscles. Physiol Rev. 52, 129–197 (1972).

    Article  CAS  Google Scholar 

  13. Gayer, C. P. & Basson, M. D. The effects of mechanical forces on intestinal physiology and pathology. Cell Signal. 21, 1237–1244 (2009).

    Article  CAS  Google Scholar 

  14. Scholten, K. & Meng, E. Materials for microfabricated implantable devices: a review. Lab Chip 15, 4256–4272 (2015).

    Article  CAS  Google Scholar 

  15. McKee, C. T., Last, J. A., Russell, P. & Murphy, C. J. Indentation versus tensile measurements of Young's modulus for soft biological tissues. Tissue Eng. Part B Rev. 17, 154–163 (2011).

    Article  Google Scholar 

  16. Hiesinger, W. et al. Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell–derived factor 1α angiogenic therapy for acute myocardial infarction in a murine model. J. Thorac. Cardiovasc. Surg. 143, 962–966 (2012).

    Article  Google Scholar 

  17. Discher, D. & Engler, A. in ASME 2007 Summer Bioengineering Conference (ed Steinman, D. A. ) 249–250 (Keystone, 2007).

    Book  Google Scholar 

  18. Engler, A. J. et al. Myotubes differentiate optimally on substrates with tissue-like stiffness. J. Cell Biol. 165, 877–887 (2004).

    Article  Google Scholar 

  19. Goffin, J. M. et al. Focal adhesion size controls tension-dependent recruitment of α-smooth muscle actin to stress fibers. J. Cell Biol. 171, 259–268 (2006).

    Article  CAS  Google Scholar 

  20. Samani, A., Zubovits, J. & Plewes, D. Elastic moduli of normal and pathological human breast tissues: an inversion-technique-based investigation of 168 samples. Phys. Med. Biol. 52, 1555 (2007).

    Google Scholar 

  21. Wuerfel, J. et al. MR-elastography reveals degradation of tissue integrity in multiple sclerosis. Neuroimage 49, 2520–2525 (2010).

    Article  Google Scholar 

  22. Rowland, L. P. & Shneider, N. A. Amyotrophic lateral sclerosis. N. Engl. J. Med. 344, 1678–1690 (2001).

    Google Scholar 

  23. Discher, D. E., Janmey, P. & Wang, Y.-l. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139–1143 (2005).

    Article  CAS  Google Scholar 

  24. Anderson, J. M., Rodriguez, A. & Chang, D. T. Foreign body reaction to biomaterials. Semin. Immunol. 20, 86–100 (2008).

    Article  CAS  Google Scholar 

  25. Wilson, C. J., Clegg, R. E., Leavesley, D. I. & Pearcy, M. J. Mediation of biomaterial–cell interactions by adsorbed proteins: a review. Tissue Eng. 11, 1–18 (2005).

    Article  CAS  Google Scholar 

  26. Henson, P. M. The immunologic release of constituents from neutrophil leukocytes I. The role of antibody and complement on nonphagocytosable surfaces or phagocytosable particles. J. Immunol. 107, 1535–1546 (1971).

    CAS  Google Scholar 

  27. Christenson, E. M., Anderson, J. M. & Hiltner, A. Oxidative mechanisms of poly (carbonate urethane) and poly (ether urethane) biodegradation: in vivo and in vitro correlations. J. Biomed. Mater. Res. Part A 70, 245–255 (2004).

    Article  CAS  Google Scholar 

  28. Brodbeck, W. G. et al. Biomaterial adherent macrophage apoptosis is increased by hydrophilic and anionic substrates in vivo. Proc. Natl Acad. Sci. USA 99, 10287–10292 (2002).

    Article  CAS  Google Scholar 

  29. Costerton, J., Montanaro, L. & Arciola, C. Biofilm in implant infections: its production and regulation. Int. J. Artif. Organs 28, 1062–1068 (2005).

    Article  CAS  Google Scholar 

  30. Fishbein, M. C., Maclean, D. & Maroko, P. R. The histopathologic evolution of myocardial infarction. Chest 73, 843–849 (1978).

    Article  CAS  Google Scholar 

  31. Polikov, V. S., Tresco, P. A. & Reichert, W. M. Response of brain tissue to chronically implanted neural electrodes. J. Neurosci. Methods 148, 1–18 (2005).

    Article  Google Scholar 

  32. Pachter, J. S., De Vries, H. E. & Fabry, Z. The blood-brain barrier and its role in immune privilege in the central nervous system. J. Neuropathol. Exp. Neurol. 62, 593–604 (2003).

    Article  CAS  Google Scholar 

  33. Chen, R., Canales, A. & Anikeeva, P. Neural recording and modulation technologies. Nat. Rev. Mater. 2, 16093 (2017).

    Article  CAS  Google Scholar 

  34. Gerweck, L. E. & Seetharaman, K. Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res. 56, 1194–1198 (1996).

    CAS  Google Scholar 

  35. Xin, Y., Huo, K., Tao, H., Tang, G. & Chu, P. K. Influence of aggressive ions on the degradation behavior of biomedical magnesium alloy in physiological environment. Acta Biomater. 4, 2008–2015 (2008).

    Article  CAS  Google Scholar 

  36. Xu, W. et al. Increased production of reactive oxygen species contributes to motor neuron death in a compression mouse model of spinal cord injury. Spinal Cord 43, 204–213 (2005).

    Article  CAS  Google Scholar 

  37. Christenson, E. M., Dadsetan, M., Wiggins, M., Anderson, J. M. & Hiltner, A. Poly (carbonate urethane) and poly (ether urethane) biodegradation: in vivo studies. J. Biomed. Mater. Res. Part A 69, 407–416 (2004).

    Article  CAS  Google Scholar 

  38. Ali, S., Zhong, S.-P., Doherty, P. & Williams, D. Mechanisms of polymer degradation in implantable devices: I. Poly (caprolactone). Biomaterials 14, 648–656 (1993).

    Article  CAS  Google Scholar 

  39. Ali, S., Doherty, P. & Williams, D. Mechanisms of polymer degradation in implantable devices. 2. Poly (DL-lactic acid). J. Biomed. Mater. Res. Part A 27, 1409–1418 (1993).

    Article  CAS  Google Scholar 

  40. Omens, J. H. Stress and strain as regulators of myocardial growth. Prog. Biophys. Mol. Biol. 69, 559–572 (1998).

    Article  CAS  Google Scholar 

  41. Buchko, C. J., Slattery, M. J., Kozloff, K. M. & Martin, D. C. Mechanical properties of biocompatible protein polymer thin films. J. Mater. Res. 15, 231–242 (2000).

    Article  CAS  Google Scholar 

  42. Garnier, F., Hajlaoui, R., Yassar, A. & Srivastava, P. All-polymer field-effect transistor realized by printing techniques. Science 265, 1674–1677 (1994).

    Article  Google Scholar 

  43. McCoul, D., Hu, W., Gao, M., Mehta, V. & Pei, Q. Recent advances in stretchable and transparent electronic materials. Adv. Electron. Mater. 2, 1500407 (2016).

    Article  CAS  Google Scholar 

  44. Wang, C., Zheng, W., Yue, Z., Too, C. O. & Wallace, G. G. Buckled, stretchable polypyrrole electrodes for battery applications. Adv. Mater. 23, 3580–3584 (2011).

    Article  CAS  Google Scholar 

  45. Yuan, W. et al. in The 14th International Symposium on: Smart Structures and Materials & Nondestructive Evaluation and Health Monitoring 65240N-65240N-65212 (International Society for Optics and Photonics, 2007).

    Google Scholar 

  46. Hansen, T. S., West, K., Hassager, O. & Larsen, N. B. Highly stretchable and conductive polymer material made from poly (3, 4-ethylenedioxythiophene) and polyurethane elastomers. Adv. Funct. Mater. 17, 3069–3073 (2007).

    Article  CAS  Google Scholar 

  47. Samba, R., Herrmann, T. & Zeck, G. PEDOT–CNT coated electrodes stimulate retinal neurons at low voltage amplitudes and low charge densities. J. Neural Eng. 12, 015914 (2015).

    Article  Google Scholar 

  48. Owens, R. M. & Malliaras, G. G. Organic electronics at the interface with biology. MRS Bull. 35, 449–456 (2010).

    Article  CAS  Google Scholar 

  49. Park, J. et al. Electromechanical cardioplasty using a wrapped elasto-conductive epicardial mesh. Sci. Transl Med. 8, 344ra86 (2016).

    Article  CAS  Google Scholar 

  50. Carpi, F., De Rossi, D., Kornbluh, R., Pelrine, R. E. & Sommer-Larsen, P. Dielectric Elastomers as Electromechanical Transducers: Fundamentals, Materials, Devices, Models and Applications of an Emerging Electroactive Polymer Technology. (Elsevier, 2011).

    Google Scholar 

  51. Hu, L., Yuan, W., Brochu, P., Gruner, G. & Pei, Q. Highly stretchable, conductive, and transparent nanotube thin films. Appl. Phys. Lett. 94, 160108 (2009).

    Google Scholar 

  52. Smart, S., Cassady, A., Lu, G. & Martin, D. The biocompatibility of carbon nanotubes. Carbon 44, 1034–1047 (2006).

    Article  CAS  Google Scholar 

  53. Tian, F., Cui, D., Schwarz, H., Estrada, G. G. & Kobayashi, H. Cytotoxicity of single-wall carbon nanotubes on human fibroblasts. Toxicol. In Vitro 20, 1202–1212 (2006).

    Article  CAS  Google Scholar 

  54. Alarifi, S., Ali, D., Verma, A., Almajhdi, F. N. & Al-Qahtani, A. A. Single-walled carbon nanotubes induce cytotoxicity and DNA damage via reactive oxygen species in human hepatocarcinoma cells. In Vitro Cell. Dev. Biol. Anim. 50, 714–722 (2014).

    Article  CAS  Google Scholar 

  55. Dong, J. & Ma, Q. Advances in mechanisms and signaling pathways of carbon nanotube toxicity. Nanotoxicology 9, 658–676 (2015).

    Article  CAS  Google Scholar 

  56. Kim, H.-J., Son, C. & Ziaie, B. A multiaxial stretchable interconnect using liquid-alloy-filled elastomeric microchannels. Appl. Phys. Lett. 92, 011904 (2008).

    Article  CAS  Google Scholar 

  57. Siegel, A. C., Bruzewicz, D. A., Weibel, D. B. & Whitesides, G. M. Microsolidics: fabrication of three-dimensional metallic microstructures in poly (dimethylsiloxane). Adv. Mater. 19, 727–733 (2007).

    Article  CAS  Google Scholar 

  58. Dickey, M. D. et al. Eutectic gallium-indium (EGaIn): a liquid metal alloy for the formation of stable structures in microchannels at room temperature. Adv. Funct. Mater. 18, 1097–1104 (2008).

    Article  CAS  Google Scholar 

  59. Khondoker, M. & Sameoto, D. Fabrication methods and applications of microstructured gallium based liquid metal alloys. Smart Mater. Struct. 25, 093001 (2016).

    Article  CAS  Google Scholar 

  60. So, J. H. et al. Reversibly deformable and mechanically tunable fluidic antennas. Adv. Funct. Mater. 19, 3632–3637 (2009).

    Article  CAS  Google Scholar 

  61. Lide, D. R. Handbook of Chemistry and Physics 88th edn (CRC Press, 2007).

    Google Scholar 

  62. Chiechi, R. C., Weiss, E. A., Dickey, M. D. & Whitesides, G. M. Eutectic gallium–indium (EGaIn): a moldable liquid metal for electrical characterization of self-assembled monolayers. Angew. Chem. Int. Ed. 120, 148–150 (2008).

    Article  Google Scholar 

  63. Jones, J., Lacour, S. P., Wagner, S. & Suo, Z. Stretchable wavy metal interconnects. J. Vac. Sci. Technol. A Vac. Surf. Films 22, 1713–1715 (2004).

    Article  CAS  Google Scholar 

  64. Lacour, S. P., Jones, J., Suo, Z. & Wagner, S. Design and performance of thin metal film interconnects for skin-like electronic circuits. IEEE Electron. Device Lett. 25, 178–180 (2004).

    Google Scholar 

  65. Chou, N., Yoo, S. & Kim, S. A largely deformable surface type neural electrode array based on PDMS. IEEE Trans. Neural Syst. Rehabil. Eng. 21, 544–553 (2013).

    Article  Google Scholar 

  66. Graudejus, O., Yu, Z., Jones, J., Morrison, B. & Wagner, S. Characterization of an elastically stretchable microelectrode array and its application to neural field potential recordings. J. Electrochem. Soc. 155, P85–P94 (2009).

    Article  CAS  Google Scholar 

  67. Sun, Y., Choi, W. M., Jiang, H., Huang, Y. Y. & Rogers, J. A. Controlled buckling of semiconductor nanoribbons for stretchable electronics. Nat. Nanotechnol. 1, 201–207 (2006).

    Article  CAS  Google Scholar 

  68. Khang, D.-Y., Jiang, H., Huang, Y. & Rogers, J. A. A stretchable form of single-crystal silicon for high-performance electronics on rubber substrates. Science 311, 208–212 (2006).

    Article  CAS  Google Scholar 

  69. Park, S. I. et al. Theoretical and experimental studies of bending of inorganic electronic materials on plastic substrates. Adv. Funct. Mater. 18, 2673–2684 (2008).

    Article  CAS  Google Scholar 

  70. Xu, S. et al. Assembly of micro/nanomaterials into complex, three-dimensional architectures by compressive buckling. Science 347, 154–158 (2015). In this article, a method for creating stretchable 3D structures is presented. These structures could be used to create stretchable flexible 3D electronics.

    Article  CAS  Google Scholar 

  71. Xu, J. et al. Highly stretchable polymer semiconductor films through the nanoconfinement effect. Science 355, 59–64 (2017).

    Article  CAS  Google Scholar 

  72. Oh, J. Y. et al. Intrinsically stretchable and healable semiconducting polymer for organic transistors. Nature 539, 411–415 (2016).

    Article  CAS  Google Scholar 

  73. Lide, D. R. Handbook of Chemistry and Physics 86th edn (CRC Press, 2005).

    Google Scholar 

  74. Gonzalez, M. et al. in EuroSimE 2007 — International Conference on Thermal, Mechanical and Multi-Physics Simulation Experiments in Microelectronics and Micro-Systems PID83 (London, 2007).

    Google Scholar 

  75. Gonzalez, M. et al. Design and performance of metal conductors for stretchable electronic circuits. Circuit World 35, 22–29 (2009).

    Article  CAS  Google Scholar 

  76. Fan, J. A. et al. Fractal design concepts for stretchable electronics. Nat. Commun. 5, 3266 (2014).

    Article  CAS  Google Scholar 

  77. Kim, D. H. et al. Epidermal electronics. Science 333, 838–843 (2011).

    Article  CAS  Google Scholar 

  78. Xu, L. et al. 3D multifunctional integumentary membranes for spatiotemporal cardiac measurements and stimulation across the entire epicardium. Nat. Commun. 5, 3329 (2014).

    Article  CAS  Google Scholar 

  79. Kim, D.-H. et al. Materials for multifunctional balloon catheters with capabilities in cardiac electrophysiological mapping and ablation therapy. Nat. Mater. 10, 316–323 (2011).

    Article  CAS  Google Scholar 

  80. Song, Y. M. et al. Digital cameras with designs inspired by the arthropod eye. Nature 497, 95–99 (2013).

    Article  CAS  Google Scholar 

  81. Huang, X. et al. Stretchable, wireless sensors and functional substrates for epidermal characterization of sweat. Small 10, 3083–3090 (2014).

    Article  CAS  Google Scholar 

  82. Webb, R. C. et al. Ultrathin conformal devices for precise and continuous thermal characterization of human skin. Nat. Mater. 12, 938–944 (2013).

    Article  CAS  Google Scholar 

  83. Norton, J. J. et al. Soft, curved electrode systems capable of integration on the auricle as a persistent brain-computer interface. Proc. Natl Acad. Sci. USA 112, 3920–3925 (2015).

    Article  CAS  Google Scholar 

  84. Bareket, L. et al. Temporary-tattoo for long-term high fidelity biopotential recordings. Sci. Rep. 6, 25727 (2016).

    Article  CAS  Google Scholar 

  85. Kim, D.-H. et al. Electronic sensor and actuator webs for large-area complex geometry cardiac mapping and therapy. Proc. Natl Acad. Sci. USA 109, 19910–19915 (2012). This article presents an example of how flexible electronics can interact with internal organs and how they are fabricated so that they adapt to the organ topography.

    Article  CAS  Google Scholar 

  86. Chung, H. J. et al. Stretchable, multiplexed pH sensors with demonstrations on rabbit and human hearts undergoing ischemia. Adv. Healthcare Mater. 3, 59–68 (2014).

    Article  CAS  Google Scholar 

  87. Lendlein, A. & Langer, R. Biodegradable, elastic shape-memory polymers for potential biomedical applications. Science 296, 1663–1666 (2002).

    Article  Google Scholar 

  88. Soppimath, K. S., Aminabhavi, T. M., Kulkarni, A. R. & Rudzinski, W. E. Biodegradable polymeric nanoparticles as drug delivery devices. J. Control. Release 70, 1–20 (2001).

    Article  CAS  Google Scholar 

  89. Miyamoto, H. et al. Biodegradable scleral implant for intravitreal controlled release of fluconazole. Curr. Res. 16, 930–935 (1997).

    CAS  Google Scholar 

  90. Venkatraman, S. S., Tan, L. P., Joso, J. F. D., Boey, Y. C. F. & Wang, X. Biodegradable stents with elastic memory. Biomaterials 27, 1563–1568 (2006).

    Article  CAS  Google Scholar 

  91. Hermawan, H., Dubé, D. & Mantovani, D. Developments in metallic biodegradable stents. Acta Biomater. 6, 1683–1687 (2010).

    Google Scholar 

  92. Eppley, B. L. Use of resorbable plates and screws in pediatric facial fractures. J. Oral Maxillofacial Surg. 63, 385–391 (2005).

    Article  Google Scholar 

  93. Irimia-Vladu, M. et al. Biocompatible and biodegradable materials for organic field-effect transistors. Adv. Funct. Mater. 20, 4069–4076 (2010).

    Article  CAS  Google Scholar 

  94. Bettinger, C. J. & Bao, Z. Organic thin-film transistors fabricated on resorbable biomaterial substrates. Adv. Mater. 22, 651–655 (2010).

    Article  CAS  Google Scholar 

  95. Fu, K. et al. Transient rechargeable batteries triggered by cascade reactions. Nano Lett. 15, 4664–4671 (2015).

    Article  CAS  Google Scholar 

  96. Yin, L. et al. Materials, designs, and operational characteristics for fully biodegradable primary batteries. Adv. Mater. 26, 3879–3884 (2014).

    Article  CAS  Google Scholar 

  97. Bae, H. et al. Physically transient memory on a rapidly dissoluble paper for security application. Sci. Rep. 6, 38324 (2016).

    Article  CAS  Google Scholar 

  98. Hwang, S. W. et al. A physically transient form of silicon electronics. Science 337, 1630–1634 (2012). This article presents a shift in bioresorbable electronics in which silicon-based circuit components can be manufactured to have a transient lifetime.

    Article  CAS  Google Scholar 

  99. Yin, L. et al. Dissolvable metals for transient electronics. Adv. Funct. Mater. 24, 645–658 (2014).

    Article  CAS  Google Scholar 

  100. Kim, D.-H. et al. Silicon electronics on silk as a path to bioresorbable, implantable devices. Appl. Phys. Lett. 95, 133701 (2009).

    Article  CAS  Google Scholar 

  101. Wu, F. et al. Silk-backed structural optimization of high-density flexible intracortical neural probes. J. Microelectromechan. Syst. 24, 62–69 (2015).

    Article  CAS  Google Scholar 

  102. Tao, H. et al. Silk-based resorbable electronic devices for remotely controlled therapy and in vivo infection abatement. Proc. Natl Acad. Sci. USA 111, 17285–17289 (2014).

    Google Scholar 

  103. Jin, H. J. et al. Water-stable silk films with reduced β-sheet content. Adv. Funct. Mater. 15, 1241–1247 (2005).

    Article  CAS  Google Scholar 

  104. Hwang, S. W. et al. Materials for bioresorbable radio frequency electronics. Adv. Mater. 25, 3526–3531 (2013).

    Article  CAS  Google Scholar 

  105. Kim, D.-H. et al. Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. Nat. Mater. 9, 511–517 (2010).

    Article  CAS  Google Scholar 

  106. Makadia, H. K. & Siegel, S. J. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers 3, 1377–1397 (2011).

    Article  CAS  Google Scholar 

  107. Acar, H. et al. Study of physically transient insulating materials as a potential platform for transient electronics and bioelectronics. Adv. Funct. Mater. 24, 4135–4143 (2014).

    Article  CAS  Google Scholar 

  108. Hwang, S.-W. et al. Biodegradable elastomers and silicon nanomembranes/nanoribbons for stretchable, transient electronics, and biosensors. Nano Lett. 15, 2801–2808 (2015).

    Article  CAS  Google Scholar 

  109. Martin, C., Dejardin, T., Hart, A., Riehle, M. O. & Cumming, D. R. Directed nerve regeneration enabled by wirelessly powered electrodes printed on a biodegradable polymer. Adv. Healthcare Mater. 3, 1001–1006 (2014).

    Article  CAS  Google Scholar 

  110. Hwang, S. W. et al. High-performance biodegradable/transient electronics on biodegradable polymers. Adv. Mater. 26, 3905–3911 (2014).

    Article  CAS  Google Scholar 

  111. Irimia-Vladu, M., Głowacki, E. D., Voss, G., Bauer, S. & Sariciftci, N. S. Green and biodegradable electronics. Mater. Today 15, 340–346 (2012).

    Article  CAS  Google Scholar 

  112. Yin, L. et al. Mechanisms for hydrolysis of silicon nanomembranes as used in bioresorbable electronics. Adv. Mater. 27, 1847–1854 (2015).

    Google Scholar 

  113. Lee, G. et al. in ECS Meeting Abstracts 77 (The Electrochemical Society, 2017).

    Google Scholar 

  114. Hwang, S. W. et al. Materials and fabrication processes for transient and bioresorbable high-performance electronics. Adv. Funct. Mater. 23, 4087–4093 (2013).

    Article  CAS  Google Scholar 

  115. Yu, K. J. et al. Bioresorbable silicon electronics for transient spatiotemporal mapping of electrical activity from the cerebral cortex. Nat. Mater. 15, 782–791 (2016).

    Article  CAS  Google Scholar 

  116. Kang, S. K. et al. Bioresorbable silicon electronic sensors for the brain. Nature 530, 71–76 (2016).

    Article  CAS  Google Scholar 

  117. Gao, Z. et al. Silicon nanowire arrays for label-free detection of DNA. Anal. Chem. 79, 3291–3297 (2007).

    Article  CAS  Google Scholar 

  118. Patolsky, F., Zheng, G. & Lieber, C. M. Fabrication of silicon nanowire devices for ultrasensitive, label-free, real-time detection of biological and chemical species. Nat. Protoc. 1, 1701–1714 (2006).

    Article  CAS  Google Scholar 

  119. Zheng, G., Patolsky, F., Cui, Y., Wang, W. U. & Lieber, C. M. Multiplexed electrical detection of cancer markers with nanowire sensor arrays. Nat. Biotechnol. 23, 1294–1301 (2005).

    Article  CAS  Google Scholar 

  120. Park, C. W. et al. Thermally triggered degradation of transient electronic devices. Adv. Mater. 27, 3783–3788 (2015).

    Article  CAS  Google Scholar 

  121. Troyk, P. R. Injectable electronic identification, monitoring, and stimulation systems. Annu. Rev. Biomed. Eng. 1, 176–209 (1999).

    Article  Google Scholar 

  122. Johannessen, E. et al. Toward an injectable continuous osmotic glucose sensor. J. Diabetes Sci. Technol. 4, 882–892 (2010).

    Article  Google Scholar 

  123. Liu, J. et al. Syringe-injectable electronics. Nat. Nanotechnol. 10, 629–636 (2015). This article presents the first example of electronics flexible enough to be injected through a syringe.

    Article  CAS  Google Scholar 

  124. Xie, C. et al. Three-dimensional macroporous nanoelectronic networks as minimally invasive brain probes. Nat. Mater. 14, 1286–1292 (2015).

    Article  CAS  Google Scholar 

  125. Kim, T.-i. et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 340, 211–216 (2013).

    Article  CAS  Google Scholar 

  126. Koh, A. et al. Ultrathin injectable sensors of temperature, thermal conductivity, and heat capacity for cardiac ablation monitoring. Adv. Healthcare Mater. 5, 373–381 (2016).

    Article  CAS  Google Scholar 

  127. Luan, L. et al. Ultraflexible nanoelectronic probes form reliable, glial scar–free neural integration. Sci. Adv. 3, e1591966 (2017).

    Article  CAS  Google Scholar 

  128. Jiang, Y. et al. Heterogeneous silicon mesostructures for lipid-supported bioelectric interfaces. Nature Mater. 15, 1023–1030 (2016).

    Article  CAS  Google Scholar 

  129. McCall, J. G. et al. Fabrication of flexible, multimodal light-emitting devices for wireless optogenetics. Nature Protoc. 8, 2413 (2013).

    Article  CAS  Google Scholar 

  130. Hong, G. et al. Syringe injectable electronics: precise targeted delivery with quantitative input/output connectivity. Nano Lett. 15, 6979–6984 (2015).

    Article  CAS  Google Scholar 

  131. Schuhmann, T. G., Yao, J., Hong, G., Fu, T.-M. & Lieber, C. M. Syringe-injectable electronics with a plug-and-play input/output interface. Nano Lett. 17, 5836–5842 (2017).

    Article  CAS  Google Scholar 

  132. Zhou, T. et al. Syringe-injectable mesh electronics integrate seamlessly with minimal chronic immune response in the brain. Proc. Natl Acad. Sci. USA 114, 5894–5899 (2017).

    Article  CAS  Google Scholar 

  133. Fu, T.-M. et al. Stable long-term chronic brain mapping at the single-neuron level. Nat. Methods 13, 875–882 (2016).

    Article  CAS  Google Scholar 

  134. Duan, X. et al. Intracellular recordings of action potentials by an extracellular nanoscale field-effect transistor. Nat. Nanotechnol. 7, 173–178 (2012).

    CAS  Google Scholar 

  135. Tian, B. et al. Three-dimensional, flexible nanoscale field-effect transistors as localized bioprobes. Science 329, 830–834 (2010).

    Article  CAS  Google Scholar 

  136. Landa, N. et al. Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat. Circulation 117, 1388–1396 (2008).

    Article  CAS  Google Scholar 

  137. Dvir, T., Timko, B. P., Kohane, D. S. & Langer, R. Nanotechnological strategies for engineering complex tissues. Nat. Nanotechnol. 6, 13–22 (2011).

    Article  CAS  Google Scholar 

  138. Zsedenyi, A. et al. Gold nanoparticle-filled biodegradable photopolymer scaffolds induced muscle remodeling: in vitro and in vivo findings. Mater. Sci. Eng. C 72, 625–630 (2017).

    Article  CAS  Google Scholar 

  139. Dvir, T. et al. Nanowired three-dimensional cardiac patches. Nat. Nanotechnol. 6, 720–725 (2011).

    Article  CAS  Google Scholar 

  140. Shevach, M., Maoz, B. M., Feiner, R., Shapira, A. & Dvir, T. Nanoengineering gold particle composite fibers for cardiac tissue engineering. J. Mater. Chem. B 1, 5210–5217 (2013).

    Article  CAS  Google Scholar 

  141. Fleischer, S., Shevach, M., Feiner, R. & Dvir, T. Coiled fiber scaffolds embedded with gold nanoparticles improve the performance of engineered cardiac tissues. Nanoscale 6, 9410–9414 (2014).

    Article  CAS  Google Scholar 

  142. Shevach, M., Fleischer, S., Shapira, A. & Dvir, T. Gold nanoparticle-decellularized matrix hybrids for cardiac tissue engineering. Nano Lett. 14, 5792–5796 (2014).

    Article  CAS  Google Scholar 

  143. Baranes, K., Shevach, M., Shefi, O. & Dvir, T. Gold nanoparticle-decorated scaffolds promote neuronal differentiation and maturation. Nano Lett. 16, 2916–2920 (2015).

    Article  CAS  Google Scholar 

  144. Radisic, M. et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl Acad. Sci. USA 101, 18029–18034 (2004).

    Article  CAS  Google Scholar 

  145. Abbott, J. et al. CMOS nanoelectrode array for all-electrical intracellular electrophysiological imaging. Nat. Nanotechnol. 12, 460–466 (2017).

    Article  CAS  Google Scholar 

  146. Lind, J. U. et al. Instrumented cardiac microphysiological devices via multimaterial three-dimensional printing. Nat. Mater. 16, 303–308 (2016).

    Article  CAS  Google Scholar 

  147. Cho, S. & Yoon, J.-Y. Organ-on-a-chip for assessing environmental toxicants. Curr. Opin. Biotechnol. 45, 34–42 (2017).

    Article  CAS  Google Scholar 

  148. Ribas, J. et al. Cardiovascular organ-on-a-chip platforms for drug discovery and development. Appl. In Vitro Toxicol. 2, 82–96 (2016).

    Article  Google Scholar 

  149. Huh, D. et al. Reconstituting organ-level lung functions on a chip. Science 328, 1652–1658 (2010).

    Article  CAS  Google Scholar 

  150. Wang, Z., Samanipour, R., Koo, K.-i. & Kim, K. Organ-on-a-chip platforms for drug delivery and cell characterization: a review. Sensors Mater. 27, 487–506 (2015).

    CAS  Google Scholar 

  151. Zheng, F. et al. Organ-on-a-chip systems: microengineering to biomimic living systems. Small 12, 2253–2282 (2016).

    Article  CAS  Google Scholar 

  152. Tian, B. et al. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat. Mater. 11, 986–994 (2012). This is the first example of the integration of engineered tissues with electronics for sensing tissue function.

    Article  CAS  Google Scholar 

  153. Feiner, R. et al. Engineered hybrid cardiac patches with multifunctional electronics for online monitoring and regulation of tissue function. Nat. Mater. 15, 679–685 (2016). This article describes the first example of the integration of electronics with engineered tissues for regulating their function by sensing, stimulating and releasing drugs.

    Article  CAS  Google Scholar 

  154. Dai, X., Zhou, W., Gao, T., Liu, J. & Lieber, C. M. Three-dimensional mapping and regulation of action potential propagation in nanoelectronics-innervated tissues. Nat. Nanotechnol. 11, 776–782 (2016).

    Article  CAS  Google Scholar 

  155. Yan, Z. et al. Mechanical assembly of complex, 3D mesostructures from releasable multilayers of advanced materials. Sci. Adv. 2, e1591014 (2016).

    Article  CAS  Google Scholar 

  156. Lazarus, A. Remote, wireless, ambulatory monitoring of implantable pacemakers, cardioverter defibrillators, and cardiac resynchronization therapy systems: analysis of a worldwide database. Pacing Clin. Electrophysiol. 30, S2–S12 (2007).

    Article  Google Scholar 

  157. Luo, Z. et al. Atomic gold–enabled three-dimensional lithography for silicon mesostructures. Science 348, 1451–1455 (2015).

    Article  CAS  Google Scholar 

  158. Zimmerman, J. F. et al. Cellular uptake and dynamics of unlabeled freestanding silicon nanowires. Sci. Adv. 2, e1591039 (2016).

    Article  CAS  Google Scholar 

  159. Dagdeviren, C. et al. Conformal piezoelectric energy harvesting and storage from motions of the heart, lung, and diaphragm. Proc. Natl Acad. Sci. USA 111, 1927–1932 (2014). This article presents energy harvesting from internal organs through piezoelectric components on a flexible device.

    Article  CAS  Google Scholar 

  160. Deisseroth, K. Optogenetics. Nat. Methods 8, 26–29 (2011).

    Article  CAS  Google Scholar 

  161. Wang, Y. et al. Wearable and highly sensitive graphene strain sensors for human motion monitoring. Adv. Funct. Mater. 24, 4666–4670 (2014).

    Article  CAS  Google Scholar 

  162. Dagdeviren, C. et al. Flexible piezoelectric devices for gastrointestinal motility sensing. Nat. Biomed. Eng. 1, 807–817 (2017).

    Article  Google Scholar 

  163. Merrill, D. R., Bikson, M. & Jefferys, J. G. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 170–198 (2005).

    Article  Google Scholar 

  164. Cogan, S. F. Neural stimulation and recording electrodes. Annu. Rev. Biomed. Eng. 10, 275–309 (2008).

    Article  CAS  Google Scholar 

  165. Zhao, Y. et al. Patch clamp technique: review of the current state of the art and potential contributions from nanoengineering. Proc. Inst. Mechan. Eng. Part N J. Nanomater Nanoeng. Nanosyst. 222, 1–11 (2008).

    Google Scholar 

  166. Spira, M. E. & Hai, A. Multi-electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. 8, 83–94 (2013).

    Article  CAS  Google Scholar 

  167. Shmoel, N. et al. Multisite electrophysiological recordings by self-assembled loose-patch-like junctions between cultured hippocampal neurons and mushroom-shaped microelectrodes. Sci. Rep. 6, 27110 (2016).

    Article  CAS  Google Scholar 

  168. Hai, A., Shappir, J. & Spira, M. E. In-cell recordings by extracellular microelectrodes. Nat. Methods 7, 200–202 (2010).

    Article  CAS  Google Scholar 

  169. Andreev, A., Gersuni, G. & Volokhov, A. On the electrical excitability of the human ear: on the effect of alternating currents on the affected auditory apparatus. J. Physiol. USSR 18, 250–265 (1935).

    Google Scholar 

  170. Djourno, A. & Eyries, C. Auditory prosthesis by means of a distant electrical stimulation of the sensory nerve with the use of an indwelt coiling. La Presse Méd. 65, 1417–1417 (1957).

    CAS  Google Scholar 

  171. Stokes, K. B. Drug dispensing body implantable lead. US Patent 4506680 (1985).

  172. Benabid, A.-L., Pollak, P., Louveau, A., Henry, S. & De Rougemont, J. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Stereotact. Funct. Neurosurgery 50, 344–346 (1987).

    Article  CAS  Google Scholar 

  173. Gelbart, D. & Lichtenstein, S. V. Self-powered leadless pacemaker. US Patent 20070276444 A1 (2006).

  174. Gozen, B. A., Tabatabai, A. O., Burak Ozdoganlar, O. B. & Majidi, C. High-density soft-matter electronics with micron-scale line width. Adv. Mater. 26, 5211–5216 (2014).

    Article  CAS  Google Scholar 

  175. Nguyen, J. K. et al. Mechanically-compliant intracortical implants reduce the neuroinflammatory response. J. Neural Eng. 11, 056014 (2014).

    Article  Google Scholar 

  176. Cobbe, S. & Poole-Wilson, P. The time of onset and severity of acidosis in myocardial ischaemia. J. Mol. Cell. Cardiol. 12, 745–760 (1980).

    Article  CAS  Google Scholar 

  177. Van Der Vliet, A. & Bast, A. Role of reactive oxygen species in intestinal diseases. Free Radic. Biol. Med. 12, 499–513 (1992).

    Article  CAS  Google Scholar 

  178. Kusters, J. G., van Vliet, A. H. & Kuipers, E. J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19, 449–490 (2006).

    Article  CAS  Google Scholar 

  179. Halliwell, B. Reactive oxygen species and the central nervous system. J. Neurochem. 59, 1599–1613 (1992).

    Article  Google Scholar 

  180. Yeh, W.-C. et al. Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med. Biol. 28, 467–474 (2002).

    Article  Google Scholar 

  181. Wada, T. et al. Correlation of ultrasound-measured common carotid artery stiffness with pathological findings. Arterioscler. Thromb. 14, 479–482 (1994).

    Article  CAS  Google Scholar 

  182. Tilleman, T. R., Neumann, M. H. & Tilleman, M. M. Analyses of skin waste during excision of benign skin lesions: is the surgical ellipse cut necessary? Plast. Reconstructive Surg. 119, 2343–2345 (2007).

    Article  CAS  Google Scholar 

  183. Vey, E. et al. Degradation mechanism of poly (lactic-co-glycolic) acid block copolymer cast films in phosphate buffer solution. Polymer Degrad. Stabil. 93, 1859–1876 (2008).

    Article  CAS  Google Scholar 

  184. Li, X., Kanjwal, M. A., Lin, L. & Chronakis, I. S. Electrospun polyvinyl-alcohol nanofibers as oral fast-dissolving delivery system of caffeine and riboflavin. Colloids Surf. B 103, 181–188 (2013).

    Article  CAS  Google Scholar 

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Acknowledgements

R.F. thanks the Clore Scholarship programme, Marian Gertner Institute for Medical Nanosystems Fellowship and the Argentinian friends of Tel Aviv University. T.D. acknowledges support from the European Research Council (ERC) Starting Grant 637943, the Slezak Foundation and the Israeli Science Foundation (700/13).

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Authors and Affiliations

  1. The School for Molecular Cell Biology and Biotechnology, Faculty of Life Sciences, Tel Aviv University,

    Ron Feiner & Tal Dvir

  2. The Center for Nanoscience and Nanotechnology, Tel Aviv University,

    Ron Feiner & Tal Dvir

  3. Department of Materials Science and Engineering, Faculty of Engineering, Tel Aviv University,

    Tal Dvir

  4. Sagol School of Neuroscience, Tel Aviv University,

    Tal Dvir

  5. Sagol Center for Regenerative Biotechnology, Tel Aviv University, Tel Aviv, 69978, Israel

    Tal Dvir

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  1. Ron Feiner
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Both authors contributed equally to the preparation of this manuscript.

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Correspondence to Tal Dvir.

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Feiner, R., Dvir, T. Tissue–electronics interfaces: from implantable devices to engineered tissues. Nat Rev Mater 3, 17076 (2018). https://doi.org/10.1038/natrevmats.2017.76

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