Next generation bioelectronics: Advances in fabrication coupled with clever chemistries enable the effective integration of biomaterials and organic conductors

Organic bioelectronics is making an enormous impact in the field of tissue engineering, providing not just biocompatible, but biofunctional conducting material platforms. For their true potential to be reached, it is critical to integrate organic conductors with other biopolymers in a targeted manner, allowing the development of devices and scaffold architectures capable of delivering a number of physical, chemical, and electrical stimuli. Herein, we provide an overview of the methods currently being employed to tailor organic conductors for bioapplications, with a focus on the development of fabrication techniques vital to the development of the next generation of intelligent bionic devices.

[1]  J. Kucińska-Lipka,et al.  Fabrication of polyurethane and polyurethane based composite fibres by the electrospinning technique for soft tissue engineering of cardiovascular system. , 2015, Materials science & engineering. C, Materials for biological applications.

[2]  G. Wallace,et al.  A reactive wet spinning approach to polypyrrole fibres , 2011 .

[3]  Fan Yang,et al.  Robust cell migration and neuronal growth on pristine carbon nanotube sheets and yarns , 2007, Journal of biomaterials science. Polymer edition.

[4]  D. Mooney,et al.  Designing alginate hydrogels to maintain viability of immobilized cells. , 2003, Biomaterials.

[5]  Jae-Hong Kim,et al.  Fabrication and electrochemical properties of carbon nanotube film electrodes , 2006 .

[6]  William R. Stauffer,et al.  Polypyrrole doped with 2 peptide sequences from laminin. , 2006, Biomaterials.

[7]  G. Wallace,et al.  Creating conductive structures for cell growth: growth and alignment of myogenic cell types on polythiophenes. , 2010, Journal of biomedical materials research. Part A.

[8]  J. Pan,et al.  Investigation of Electrochemical Behavior of Stimulation'Sensing Materials for Pacemaker Electrode Applications I. Pt, Ti, and TiN Coated Electrodes , 2005 .

[9]  C. M. Li,et al.  RGD-peptide functionalized graphene biomimetic live-cell sensor for real-time detection of nitric oxide molecules. , 2012, ACS nano.

[10]  Miqin Zhang,et al.  Chitosan-alginate as scaffolding material for cartilage tissue engineering. , 2005, Journal of biomedical materials research. Part A.

[11]  H. Uehata,et al.  Initial and 6-month results of biodegradable poly-l-lactic acid coronary stents in humans. , 2000, Circulation.

[12]  Z. Yue,et al.  Influence of Biodopants on PEDOT Biomaterial Polymers: Using QCM‐D to Characterize Polymer Interactions with Proteins and Living Cells , 2014 .

[13]  A. Simmons,et al.  Biostability and biological performance of a PDMS-based polyurethane for controlled drug release. , 2008, Biomaterials.

[14]  X. Beebe,et al.  Charge injection limits of activated iridium oxide electrodes with 0.2 ms pulses in bicarbonate buffered saline (neurological stimulation application) , 1988, IEEE Transactions on Biomedical Engineering.

[15]  David J Mooney,et al.  The tensile properties of alginate hydrogels. , 2004, Biomaterials.

[16]  Wei Wang,et al.  High strength graphene oxide/polyvinyl alcohol composite hydrogels , 2011 .

[17]  Peter F. M. Choong,et al.  Chondrogenesis of Infrapatellar Fat Pad Derived Adipose Stem Cells in 3D Printed Chitosan Scaffold , 2014, PloS one.

[18]  S. Ramakrishna,et al.  In vivo study of novel nanofibrous intra-luminal guidance channels to promote nerve regeneration , 2010, Journal of neural engineering.

[19]  A Ranella,et al.  Direct laser writing of 3D scaffolds for neural tissue engineering applications , 2011, Biofabrication.

[20]  Hao Hong,et al.  Graphene: a versatile nanoplatform for biomedical applications. , 2012, Nanoscale.

[21]  Hui Hu,et al.  Chemically Functionalized Carbon Nanotubes as Substrates for Neuronal Growth. , 2004, Nano letters.

[22]  G M Clark,et al.  A multiple-electrode array for a cochlear implant , 1976, The Journal of Laryngology & Otology.

[23]  T. Maekawa,et al.  POLYMERIC SCAFFOLDS IN TISSUE ENGINEERING APPLICATION: A REVIEW , 2011 .

[24]  Joselito M. Razal,et al.  Wet‐Spun Biodegradable Fibers on Conducting Platforms: Novel Architectures for Muscle Regeneration , 2009 .

[25]  Timo Stöver,et al.  Biomaterials in cochlear implants , 2011, GMS current topics in otorhinolaryngology, head and neck surgery.

[26]  G. Spadaro,et al.  E-beam crosslinked, biocompatible functional hydrogels incorporating polyaniline nanoparticles , 2012 .

[27]  Y. Wan,et al.  Synthesis and characterization of three-dimensional porous graphene oxide/sodium alginate scaffolds with enhanced mechanical properties , 2014 .

[28]  R J Zdrahala,et al.  Biomedical Applications of Polyurethanes: A Review of Past Promises, Present Realities, and a Vibrant Future , 1999, Journal of biomaterials applications.

[29]  J. Ng,et al.  Polypyrrole-coated electrospun poly(lactic acid) fibrous scaffold: effects of coating on electrical conductivity and neural cell growth , 2014, Journal of biomaterials science. Polymer edition.

[30]  H. Mirzadeh,et al.  Corticosteroid-releasing cochlear implant: a novel hybrid of biomaterial and drug delivery system. , 2010, Journal of biomedical materials research. Part B, Applied biomaterials.

[31]  J. James,et al.  Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. , 2003, Toxicological sciences : an official journal of the Society of Toxicology.

[32]  Stephen O'Leary,et al.  The effect of polypyrrole with incorporated neurotrophin-3 on the promotion of neurite outgrowth from auditory neurons. , 2007, Biomaterials.

[33]  Gordon G. Wallace,et al.  Covalently linked biocompatible graphene/polycaprolactone composites for tissue engineering , 2013 .

[34]  Rajagopal Ramasubramaniam,et al.  Homogeneous carbon nanotube/polymer composites for electrical applications , 2003 .

[35]  Anthony Guiseppi-Elie,et al.  Electroconductive hydrogels: synthesis, characterization and biomedical applications. , 2010, Biomaterials.

[36]  J. Noth,et al.  Cytocompatibility of a novel, longitudinally microstructured collagen scaffold intended for nerve tissue repair. , 2009, Tissue engineering. Part A.

[37]  G. Wallace,et al.  Organic Bionics: WALLACE:ORGANIC BIONICS O-BK , 2012 .

[38]  Gordon G Wallace,et al.  A Conducting‐Polymer Platform with Biodegradable Fibers for Stimulation and Guidance of Axonal Growth , 2009, Advanced materials.

[39]  Daryl R Kipke,et al.  Conducting polymers on hydrogel-coated neural electrode provide sensitive neural recordings in auditory cortex. , 2010, Acta biomaterialia.

[40]  Chi-Hwa Wang,et al.  Optimized bone regeneration based on sustained release from three‐dimensional fibrous PLGA/HAp composite scaffolds loaded with BMP‐2 , 2008, Biotechnology and bioengineering.

[41]  Wei Zhu,et al.  3D nano/microfabrication techniques and nanobiomaterials for neural tissue regeneration. , 2014, Nanomedicine.

[42]  George G. Malliaras,et al.  Control of cell migration using a conducting polymer device , 2010 .

[43]  K. Shakesheff,et al.  Controlled release of BMP‐2 from a sintered polymer scaffold enhances bone repair in a mouse calvarial defect model , 2014, Journal of tissue engineering and regenerative medicine.

[44]  Erik Dujardin,et al.  Young's modulus of single-walled nanotubes , 1998 .

[45]  Christine E. Schmidt,et al.  Conducting polymers in biomedical engineering , 2007 .

[46]  Yen Wei,et al.  Electrospinning polyaniline-contained gelatin nanofibers for tissue engineering applications. , 2006, Biomaterials.

[47]  Yi‐Cheng Huang,et al.  Surface modification and characterization of chitosan or PLGA membrane with laminin by chemical and oxygen plasma treatment for neural regeneration. , 2007, Journal of biomedical materials research. Part A.

[48]  Feng Yan,et al.  The Application of Organic Electrochemical Transistors in Cell‐Based Biosensors , 2010, Advanced materials.

[49]  Gordon G Wallace,et al.  Biocompatibility of immobilized aligned carbon nanotubes. , 2011, Small.

[50]  S. Panero,et al.  Synthesis and characterization of new electroactive polypyrrole-chondroitin sulphate A substrates. , 2008, Bioelectrochemistry.

[51]  A. Concheiro,et al.  Hot melt poly-ε-caprolactone/poloxamine implantable matrices for sustained delivery of ciprofloxacin. , 2012, Acta biomaterialia.

[52]  Gordon G Wallace,et al.  Physical surface and electromechanical properties of doped polypyrrole biomaterials. , 2010, Biomaterials.

[53]  Yoshihisa Suzuki,et al.  Cat peripheral nerve regeneration across 50 mm gap repaired with a novel nerve guide composed of freeze-dried alginate gel , 1999, Neuroscience Letters.

[54]  David C. Martin,et al.  Conducting polymers grown in hydrogel scaffolds coated on neural prosthetic devices. , 2004, Journal of biomedical materials research. Part A.

[55]  James D. Weiland,et al.  In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes , 2002, IEEE Transactions on Biomedical Engineering.

[56]  Ying Wang,et al.  Preparation, Structure, and Electrochemical Properties of Reduced Graphene Sheet Films , 2009 .

[57]  G. Wallace,et al.  An erodible polythiophene-based composite for biomedical applications , 2011 .

[58]  Gordon G Wallace,et al.  Skeletal muscle cell proliferation and differentiation on polypyrrole substrates doped with extracellular matrix components. , 2009, Biomaterials.

[59]  E. Sachlos,et al.  Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. , 2003, European cells & materials.

[60]  R. Hamers,et al.  Electrically Addressable Biomolecular Functionalization of Carbon Nanotube and Carbon Nanofiber Electrodes , 2004 .

[61]  M. Abidian,et al.  Conducting‐Polymer Nanotubes for Controlled Drug Release , 2006, Advanced materials.

[62]  L. M. Lira,et al.  Conducting polymer–hydrogel composites for electrochemical release devices: Synthesis and characterization of semi-interpenetrating polyaniline–polyacrylamide networks , 2005 .

[63]  Ioannis S. Chronakis,et al.  Conductive polypyrrole nanofibers via electrospinning: Electrical and morphological properties , 2006 .

[64]  David C. Martin,et al.  In vivo studies of polypyrrole/peptide coated neural probes. , 2003, Biomaterials.

[65]  S. Hsu,et al.  Evaluation of chitosan-alginate-hyaluronate complexes modified by an RGD-containing protein as tissue-engineering scaffolds for cartilage regeneration. , 2004, Artificial organs.

[66]  M. Berggren,et al.  Organic electronics for precise delivery of neurotransmitters to modulate mammalian sensory function. , 2009, Nature materials.

[67]  M. Berggren,et al.  Electronic control of Ca2+ signalling in neuronal cells using an organic electronic ion pump. , 2007, Nature materials.

[68]  George G. Malliaras,et al.  Organic Electronics at the Interface with Biology , 2010 .

[69]  Jae Young Lee,et al.  Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. , 2009, Biomaterials.

[70]  P. Leleux,et al.  In vivo recordings of brain activity using organic transistors , 2013, Nature Communications.

[71]  Ilídio J Correia,et al.  Development of a new chitosan hydrogel for wound dressing , 2009, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[72]  Alwin M D Wan,et al.  Electrical control of cell density gradients on a conducting polymer surface. , 2009, Chemical communications.

[73]  J. Feijen,et al.  Injectable chitosan-based hydrogels for cartilage tissue engineering. , 2009, Biomaterials.

[74]  Seeram Ramakrishna,et al.  Electrospun biomimetic nanocomposite nanofibers of hydroxyapatite/chitosan for bone tissue engineering. , 2008, Biomaterials.

[75]  Jeong Ah Kim,et al.  Regulation of morphogenesis and neural differentiation of human mesenchymal stem cells using carbon nanotube sheets. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[76]  David C. Martin,et al.  Sustained release of dexamethasone from hydrophilic matrices using PLGA nanoparticles for neural drug delivery. , 2006, Biomaterials.

[77]  Miqin Zhang,et al.  Chitosan-alginate hybrid scaffolds for bone tissue engineering. , 2005, Biomaterials.

[78]  P. W. Wang,et al.  Electrospun collagen-chitosan nanofiber: a biomimetic extracellular matrix for endothelial cell and smooth muscle cell. , 2010, Acta biomaterialia.

[79]  Gregory R. D. Evans,et al.  Clinical long-term in vivo evaluation of poly(L-lactic acid) porous conduits for peripheral nerve regeneration , 2000, Journal of biomaterials science. Polymer edition.

[80]  D. Poncelet,et al.  Microencapsulation of DNA Within alginate microspheres and crosslinked chitosan membranes for in vivo application , 1995, Applied biochemistry and biotechnology.

[81]  Y. Liu,et al.  Guidance of neurite outgrowth on aligned electrospun polypyrrole/poly(styrene-beta-isobutylene-beta-styrene) fiber platforms. , 2010, Journal of biomedical materials research. Part A.

[82]  C. Pande Thermoplastic Polyurethanes as Insulating Materials for Long‐Life Cardiac Pacing Leads , 1983, Pacing and clinical electrophysiology : PACE.

[83]  I. Fischer,et al.  Peptide-modified Alginate Surfaces as a Growth Permissive Substrate for Neurite Outgrowth , 2004 .

[84]  T.L. Rose,et al.  Electrical stimulation with Pt electrodes. VIII. Electrochemically safe charge injection limits with 0.2 ms pulses (neuronal application) , 1990, IEEE Transactions on Biomedical Engineering.

[85]  A. Mata,et al.  Characterization of Polydimethylsiloxane (PDMS) Properties for Biomedical Micro/Nanosystems , 2005, Biomedical microdevices.

[86]  C. V. van Blitterswijk,et al.  Chitosan scaffolds containing hyaluronic acid for cartilage tissue engineering. , 2011, Tissue engineering. Part C, Methods.

[87]  R Langer,et al.  Stimulation of neurite outgrowth using an electrically conducting polymer. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[88]  R. Superfine,et al.  Bending and buckling of carbon nanotubes under large strain , 1997, Nature.

[89]  Gordon G. Wallace,et al.  Inkjet printed polypyrrole/collagen scaffold: A combination of spatial control and electrical stimulation of PC12 cells , 2012 .

[90]  P. Calvert,et al.  Inkjet and extrusion printing of conducting poly(3,4-ethylenedioxythiophene) tracks on and embedded in biopolymer materials , 2011 .