Conductive polymers: Towards a smart biomaterial for tissue engineering

Acta Biomaterialia

Volumn 10, Issue 6, 2014, Pages 2341-2353

  Balint, Richard ^a   Cassidy, Nigel J ^b   Cartmell, Sarah H ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b KEELE UNIVERSITY   (United Kingdom)

Author keywords

Biocompatibility; Conductive polymer; Drug release; Polyaniline; Polypyrrole

Indexed keywords

CONTROLLED DRUG DELIVERY; FUEL CELLS; PHYSICAL PROPERTIES; POLYANILINE; POLYMERIC IMPLANTS; POLYPYRROLES; SCAFFOLDS (BIOLOGY); TARGETED DRUG DELIVERY; TISSUE; TISSUE REGENERATION;

COMPUTER DISPLAY; CONDUCTIVE POLYMER; DRUG RELEASE; ELECTRO ACTIVES; ENGINEERING COMMUNITY; FUNCTIONALIZATIONS; PROPERTY; SMART BIOMATERIALS; STIMULI-RESPONSIVE; TISSUES ENGINEERINGS;

BIOCOMPATIBILITY;

POLYANILINE; POLYMER; POLYPYRROLE; TISSUE SCAFFOLD; BIOMATERIAL;

ARTICLE; BIOCOMPATIBILITY; BIOSENSOR; CELL CULTURE; CONDUCTANCE; DOPING; DRUG DELIVERY DEVICE; DRUG DELIVERY SYSTEM; ELECTROSPINNING; ELECTROSTIMULATION; HUMAN; HYDROGEL; NANOELECTROMECHANICAL SYSTEM; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; TISSUE CULTURE; TISSUE ENGINEERING;

BIOCOMPATIBLE MATERIALS; POLYMERS; TISSUE ENGINEERING;

EID: 84899630592     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.02.015     Document Type: Review

References (183)

1. Lakard B, Ploux L, Anselme K, Lallemand F, Lakard S, Nardin M, et al. Effect of ultrasounds on the electrochemical synthesis of polypyrrole, application to the adhesion and growth of biological cells. Bioelectrochemistry 2009;75:148-57.
2. Ghasemi-Mobarakeh L et al. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J Tissue Eng Regen Med 2011;5:e17-35.
3. Huang L et al. Synthesis of biodegradable and electroactive multiblock polylactide and aniline pentamer copolymer for tissue engineering applications. Biomacromolecules 2008;9:850-8.
4. Rivers TJ, Hudson TW, Schmidt CE. Synthesis of a novel, biodegradable electrically conducting polymer for biomedical applications. Adv Funct Mater 2002;12:33-7.
5. Kotwal A, Schmidt CE. Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials. Biomaterials 2001;22:1055-64.
6. Lee JY, Bashur CA, Goldstein AS, Schmidt CE. Polypyrrole-coated electrospun PLGA nanofibers for neural tissue applications. Biomaterials 2009;30:4325-35.
7. Wallace GG, Smyth M, Zhao H. Conducting electroactive polymer-based biosensors. Trends Analyt Chem 1999;18:245-51.
8. Kim DH, Richardson-Burns SM, Hendricks JL, Sequera C, Martin DC. Effect of immobilized nerve growth factor on conductive polymers: electrical properties and cellular response. Adv Funct Mater 2007;17:79-86.
9. Garner B, Georgevich A, Hodgson AJ, Liu L, Wallace GG. Polypyrrole-heparin composites as stimulus-responsive substrates for endothelial cell growth. Inc. J Biomed Mater Res 1999;44:121-9.
10. Aoki T, Tanino M, Sanui K, Ogata N, Kumakura K. Secretory function of adrenal chromaffin cells cultured on polypyrrole films. Biomaterials 1996;17:1971-4.
11. Guiseppi-Elie A. Electroconductive hydrogels: synthesis, characterization and biomedical applications. Biomaterials 2010;31:2701-16.
12. Shirakawa H, Louis EJ, MacDiarmid AG, Chiang CK, Heeger AJ. Synthesis of electrically conducting organic polymers: halogen derivatives of polyacetylene, (CH)x. J Chem Soc Chem Commun 1977:578-80.
13. Ateh DD, Navsaria HA, Vadgama P. Polypyrrole-based conducting polymers and interactions with biological tissues. J R Soc Interface 2006;3:741-52.
14. Zhou DD, Cui XT, Hines A, Greenberg RJ. Conducting polymers in neural stimulation applications. In: Zhou DD, Greenbaum E, editors. Implantable neural prostheses, vol. 2. Berlin: Springer; 2010. p. 217-52.
15. Guimard NK, Gomez N, Schmidt CE. Conducting polymers in biomedical engineering. Prog Polym Sci 2007;32:876-921.
16. Cortés MT, Moreno JC. Artificial muscles based on conducting polymers. e- Polymers 2003;4:1-42.
17. Kim DH, Abidian M, Martin DC. Conducting polymers grown in hydrogel scaffolds coated on neural prosthetic devices. J Biomed Mater Res 2004;71A:577-85.
18. Guimard NKE, Sessler JL, Schmidt CE. Toward a biocompatible and biodegradable copolymer incorporating electroactive oligothiophene units. Macromolecules 2009;42:502-11.
19. Li M, Guo Y, Wei Y, MacDiarmid AG, Lelkes PI. Electrospinning polyanilinecontained gelatin nanofibers for tissue engineering applications. Biomaterials 2006;27:2705-15.
20. Liu X, Gilmore KJ, Moulton SE, Wallace GG. Electrical stimulation promotes nerve cell differentiation on polypyrrole/poly(2-methoxy-5 aniline sulfonic acid) composites. J Neural Eng 2009;6:1-10.
21. Garner B, Hodgson AJ, Wallace GG, Underwood PA. Human endothelial cell attachment to and growth on polypyrrole-heparin is fibronectin dependent. J Mater Sci Mater Med 1999;10:19-27.
22. Cui X, Hetke JE, Wiler JA, Anderson DJ, Martin DC. Electrochemical deposition and characterization of conducting polymer polypyrole/PSS on multichannel neural probes. Sens Actuator A-Phys 2001;93:8-18.
23. Lee JY, Lee JW, Schmidt CE. Neuroactive conducting scaffolds: nerve growth factor conjugation on active ester-functionalized polypyrrole. J R Soc Interface 2009;6:801-10.
24. Ateh DD, Vadgama P, Navsaria HA. Culture of human keratinocytes on polypyrrole-based conducting polymers. Tissue Eng 2006;12:645-55.
25. Bousalem S, Mangeney C, Chehimi MM, Basinska T, Miksa B, Slomkowski S. Synthesis, characterization and potential biomedical applications of Nsuccinimidyl ester functionalized, polypyrrole-coated polystyrene latex particles. Colloid Polym Sci 2004;282:1301-7.
26. Li Y, Neoh KG, Kang ET. Plasma protein adsorption and thrombus formation on surface functionalized polypyrrole with and without electrical stimulation. J Colloid Interf Sci 2004;275:488-95.
27. George PM, LaVan DA, Burdick JA, Chen CY, Liang E, Langer R. Electrically controlled drug delivery from biotin-doped conductive polypyrrole. Adv Mater 2006;18:577-81.
28. Meng S, Rouabhia M, Shi G, Zhang Z. Heparin dopant increases the electrical stability, cell adhesion, and growth of conducting polypyrrole/poly(L,Llactide) composites. J Biomed Mater Res 2008;87A:332-44.
29. Cetiner S, Kalaoglu F, Karakas H, Sarac AS. Electrospun nanofibers of polypyrrole-poly(acrylonitrile-co-vinyl acetate). Text Res J 2010;80:1784-92.
30. Akkouch A, Shi G, Zhang Z, Rouabhia M. Bioactivating electrically conducting polypyrrole with fibronectin and bovine serum albumin. J Biomed Mater Res 2010;92A:221-31.
31. Ferraz N, Strømme M, Fellstrom B, Pradhan S, Nyholm L, Mihranyan A. In vitro and in vivo toxicity of rinsed and aged nanocellulose-polypyrrole composites. J Biomed Mater Res A 2012;100a:2128-38.
32. Zhang X, Manohar SK. Bulk synthesis of polypyrrole nanofibers by a seeding approach. J Am Chem Soc 2004;126:12714-5.
33. Chronakis IS, Grapenson S, Jakob A. Conductive polypyrrole nanofibers via electrospinning: electrical and morphological properties. Polymer 2006;47:1597-603.
34. Bousalem S, Yassar A, Basinska T, Miksa B, Slomkowski S, Azioune A, et al. Synthesis, characterization and biomedical applications of functionalized polypyrrole-coated polystyrene latex particles. Polym Adv Technol 2003;14:820-5.
35. Gomez N, Schmidt CE. Nerve growth factor-immobilized polypyrrole: bioactive electrically conducting polymer for enhanced neurite extension. J Biomed Mater Res A 2007;81(1):135-49.
36. Song HK, Toste B, Ahmann K, Hoffman-Kim D, Palmore GTR. Micropatterns of positive guidance cues anchored to polypyrrole doped with polyglutamic acid: a new platform for characterizie neurite extension in complex environments. Biomaterials 2006;27:473-84.
37. Zhang Z et al. Electrically conductive biodegradable polymer composite for nerve regeneration: electricity-stimulated neurite outgrowth and axon regeneration. Artif Organs 2007;31(1):13-22.
38. Brahim S, Guiseppi-Elie A. Electroconductive hydrogels: electrical and electrochemical properties of polypyrrole-poly(HEMA) composites. Electroanalysis 2005;17:556-70.
39. Lee JW, Serna F, Nickels J, Schmidt CE. Carboxylic acid-functionalized conductive polypyrrole as a bioactive platform for cell adhesion. Biomacromolecules 2006;7:1692-5.
40. Castano H, O'Rear EA, McFetridge PS, Sikavitsas VI. Polypyrrole thin films formed by admicellar polymerization support the osteogenic differentiation of mesenchymal stem cells. Macromol Biosci 2004;4:785-94.
41. Bettinger CJ, Bruggeman JP, Misra A, Borenstein JT, Langer R. Biocompatibility of biodegradable semiconducting melanin films for nerve tissue engineering. Biomaterials 2009;30:3050-7.
42. Gomez N, Lee JY, Nickels JD, Schmidt CE. Micropatterned polypyrrole: a combination of electrical and topographical characteristics for the dtimulation of cells. Adv Funct Mater 2007;17:1645-53.
43. George PM et al. Fabrication and biocompatibility of polypyrrole implants suitable for neural prosthetics. Biomaterials 2005;26:3511-9.
44. Alikacem N, Marois Y, Zhang Z, Jakubiec B, Roy R, King MW, et al. Tissue reactions to polypyrrole-coated polyesters: a magnetic resonance relaxometry study. Artif Organs 1999;23(10):910-9.
45. Blinova NV, Stejskal J, Trchova M, Prokes J. Control of polyaniline conductivity and contact angles by partial protonation. Polym Int 2008;57:66-9.
46. Cullen DK, Patel AR, Doorish JF, Smith DH, Pfister BJ. Developing a tissueengineered neural-electrical relay using encapsulated neuronal constructs on conducting polymer fibers. J Neural Eng 2008;5:374-84.
47. Borriello A, Guarino V, Schiavo L, Alvarez-Perez MA, Ambrosio L. Optimizing PANi doped electroactive substrates as patches for the regeneration of cardiac muscle. J Mater Sci: Mater Med 2011;22:1053-62.
48. Guo Y et al. Electroactive oligoaniline-containing self-assembled monolayers for tissue engineering applications. Biomacromolecules 2007;8:3025-34.
49. Prabhakaran MP, Ghasemi-Mobarakeh L, Jin G, Ramakrishna S. Electrospun conducting polymer nanofibers and electrical stimulation of nerve stem cells. J Biosci Bioeng 2011;112:501-7.
50. Yu QZ, Shi MM, Deng M, Wang M, Chen HZ. Morphology and conductivity of polyaniline sub-micron fibers prepared by electrospinning. Mater Sci Eng BSolid 2008;150:70-6.
51. Zhang QS, Yan YH, Li SP, Feng T. Synthesis of a novel biodegradable and electroactive polyphosphazene for biomedical application. Biomed Mater 2009;4:1-9.
52. Humpolicek P, Kasparkova V, Saha P, Stejskal J. Biocompatibility of polyaniline. Synth Met 2012;162:722-7.
53. Peramo A, Urbanchek MG, Spanninga SA, Povlich LK, Cederna P, Martin DC. In situ polymerization of a conductive polymer in acellular muscle tissue constructs. Tissue Eng Part A 2008;14:423-32.
54. Thomas CA, Zong K, Schottland P, Reynolds JR. Poly(3,4- alkylenedioxypyrrole)s as highly stable aqueous-compatible conducting polymers with biomedical implications. Adv Mater 2000;12:222-5.
55. Asplund M, Thaning E, Lundberg J, Sandberg-Nordqvist AC, Kostyszyn B, Inganäs O, et al. Toxicity evaluation of PEDOT/biomolecular composites intended for neural communication electrodes. Biomed Mater 2009;4: 1-12.
56. Richardson-Burns SM, Hendricks JL, Martin DC. Electrochemical polymerization of conducting polymers in living neural tissue. J Neural Eng 2007;4:L6-L13.
57. Subramanian A, Krishnan UM, Sethuraman S. Axially aligned electrically conducting biodegradable nanofibers for neural regeneration. J Mater Sci: Mater Med 2012;23:1797-809.
58. Ravichandran R, Sundarrajan S, Venugopal JR, Mukherjee S, Ramakrishna S. Applications of conducting polymers and their issues in biomedical engineering. J R Soc Interface 2010;7:S559-79.
59. Wong JY, Langer R, Ingber DE. Electrically conducting polymers can noninvasively control the shape and growth of mammalian cells. Proc Natl Acad Sci USA 1994;91:3201-4.
60. Wallace G, Spinks G. Conducting polymers - bridging the bionic interface. Soft Matter 2007;3:665-71.
61. Bredas JL, Streer GB. Polarons, bipolarons and solitons in conductive polymers. Acc Chem Res 1985;18:309-15.
62. Pelto J et al. Electroactivity and biocompatibility of polypyrrolehyaluronic acid multi-walled carbon nanotube composite. J Biomed Mater Res 2010;93A:1056-67.
63. Dai L. Conducting polymers. In: Dai L, editor. Intelligent macromolecules for smart devices: from materials synthesis to device applications. London: Springer; 2004. p. 41-80.
64. Kaynak A, Rintoul L, George GA. Change of mechanical and electrical properties of polypyrrole films with dopant concentration and oxidative aging. Mater Res Bull 2000;35:813-24.
65. Shi G, Rouabhia M, Wang Z, Dao LH, Zhang Z. A novel electrically conductive and biodegradable composite made of polypyrrole nanoparticles and polylactide. Biomaterials 2004;25:2477-88.
66. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Ramakrishna S. Electrical stimulation of nerve cells using conductive nanofibrous scaffolds for nerve tissue engineering. Tissue Eng Part A 2009;15:3605-19.
67. Bidez III PR, Li S, Macdiarmid AG, Venancio EC, Wei Y, Lelkes PI. Polyaniline, an electroactive polymer, supports adhesion and proliferation of cardiac myoblasts. J Biomater Sci Polym Ed 2006;17:199-212.
68. Gilmore KJ et al. Skeletal muscle cell proliferation and differentiation on polypyrrole substrates doped with extracellular matrix component. Biomaterials 2009;30:5292-304.
69. Ranella A, Barberoglou M, Bakogianni S, Fotakis C, Stratakis E. Tuning cell adhesion by controlling the roughness and wettability of 3D micro/nano silicon structures. Acta Biomater 2010;6:2711-20.
70. Huang HH, Ho CT, Lee TH, Lee TL, Liao KK, Chen FL. Effect of surface roughness of ground titanium on initial cell adhesion. Biomol Eng 2004;21:93-7.
71. Deligianni DD, Katsala ND, Koutsoukos PG, Missirlis YF. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials 2001;22:87-96.
72. Rosales-Leal JI et al. Effect of roughness, wettability and morphology of engineered titanium surfaces on osteoblast-like cell adhesion. Colloid Surf A: Physicochem Eng Aspects 2010;365:222-9.
73. Collier JH, Camp JP, Hudson TW, Schmidt CE. Synthesis and characterization of polypyrrole-hyaluronic acid composite biomaterials for tissue engineering applications. J Biomed Mater Res 2000;50:574-84.
74. Ramanaviciene A, Kausaite A, Tautkus S, Ramanavicius A. Biocompatibility of polypyrrole particles: an in vivo study in mice. J Pharm Pharmacol 2007;59:311-5.
75. Fonner JM, Schmidt CE, Ren P. A combined molecular dynamics and experimental study of doped polypyrrole. Polymer 2010;51:4985-93.
76. Gelmi A, Higgins MJ, Wallace GG. Physical surface and electromechanical properties of doped polypyrrole biomaterials. Biomaterials 2010;31:1974-83.
77. Moreno JS, Panero S, Artico M, Filippini P. Synthesis and characterization of new electroactive polypyrrole-chondroitin sulphate A substrates. Bioelectrochemistry 2008;72:3-9.
78. Han DH, Lee HJ, Park SM. Electrochemistry of conductive polymers. XXXV. Electrical and morphological characteristics of polypyrrole films prepared in aqueous media studied by current sensing atomic force microscopy. Electrochim Acta 2005;50:3085-92.
79. Silk T, Hong Q, Tamm J, Compton RG. AFM studies of polypyrrole film surface morphology. I. The influence of film thickness and dopant nature. Synth Met 1998;93:59-64.
80. Hodgson AJ, Gilmore K, Small C, Wallace GG, Mackenzie IL, Aoki T, et al. Reactive supramolecular assemblies of mucopolysaccharide, polypyrrole and protein as controllable biocomposites for a new generation of "intelligent biomaterials". Supramol Sci 1994;1:77-83.
81. Tan Y, Ghandi K. Kinetics and mechanism of pyrrole chemical polymerization. Synth Met 2013;175:183-91.
82. Armes SP. Optimum reaction conditions for the polymerization of pyrrole by iron (III) chloride in aqueous solution. Synth Met 1987;20:365-71.
83. Calvo PA, Rodriguez J, Grande H, Mecerreyes D, Pomposo JA. Chemical oxidative polymerization of pyrrole in the presence of m-hydroxybenzoic acid- and m-hydroxycinnamic acid-related compounds. Synth Met 2002;126:111-6.
84. Cao Y, Andreatta A, Heeger AJ, Smith P. Influence of chemical polymerization conditions on the properties of polyaniline. Polymer 1989;30:2305-11.
85. Kudoh Y, Akami K, Matsuya Y. Chemical polymerization of 3,4- ethylenedioxythiophene using an aqueous medium containing an anionic surfactant. Synth Met 1998;98:65-70.
86. Pron A, Genoud F, Menardo C, Nechtschein M. The effect of the oxidation conditions on the chemical polymerization of polyaniline. Synth Met 1988;24:193-201.
87. Martins NCT, Moura e Silva T, Montemora MF, Fernandes JCS, Ferreira MGS. Electrodeposition and characterization of polypyrrole films on aluminium alloy 6061-T6. Electrochim Acta 2008;53:4754-63.
88. Herrasti P, Díaz L, Ocón P, Ibáñez A, Fatas E. Electrochemical and mechanical properties of polypyrrole coatings on steel. Electrochim Acta 2004;49:3693-9.
89. Choi S, Park S. Electrochemistry of conductive polymers. XXVI. Effects of electrolytes and growth methods on polyaniline morphology. J Electrochem Soc 2002;149:E26-34.
90. Li CM, Sun CQ, Chen W, Pan L. Electrochemical thin film deposition of polypyrrole on different substrates. Surf Coat Technol 2005;198:474-7.
91. Kaplin DA, Qutubuddin S. Electrochemically synthesized polypyrrole films: effects of polymerization potential and electrolyte type. Polymer 1995;36:1275-86.
92. Sutton SJ, Vaughan AS. On the morphology and growth of electrochemically polymerized polypyrrole. Polymer 1995;36:1849-57.
93. Kaynak A. Effect of synthesis parameters on the surface morphology of conducting polypyrrole films. Mater Res Bull 1997;32:271-85.
94. Patra S, Barai K, Munichandraiah N. Scanning electron microscopy studies of PEDOT prepared by various electrochemical routes. Synth Met 2008;158:430-5.
95. Mondal SK, Prasad KR, Munichandraiah N. Analysis of electrochemical impedance of polyaniline films prepared by galvanostatic, potentiostatic and potentiodynamic methods. Synth Met 2005;148:275-86.
96. Girija TC, Sangaranarayanan MV. Investigation of polyaniline-coated stainless steel electrodes for electrochemical supercapacitors. Synth Met 2006;156:244-50.
97. Zhang Z, Roy R, Dugre FJ, Tessier D, Dao LH. In vitro biocompatibility study of electrically conductive polypyrrole-coated polyester fabrics. J Biomed Mater Res 2001;57:63-71.
98. Jiang X, Marois Y, Traoré A, Tessier D, Dao LH, Guidoin R, et al. Tissue reaction to polypyrrole-coated polyester fabrics: an in vivo study in rats. Tissue Eng 2002;8:635-47.
99. Tessier D, Dao LH, Zhang Z, King MW, Guidoin R. Polymerization and surface analysis of electrically-conductive polypyrrole on surface-activated polyester fabrics for biomedical applications. J Biomater Sci Polym Ed 2000;11:87-99.
100. Wang Z, Roberge C, Wan Y, Dao LH, Guidoin R, Zhang Z. A biodegradable electrical bioconductor made of polypyrrole nanoparticle/poly(D,L-lactide) composite: a preliminary in vitro biostability study. J Biomed Mater Res 2003;66A:738-46.
101. Wang Z et al. In vivo evaluation of a novel electrically conductive polypyrrole/poly(D,L-lactide) composite and polypyrrolecoated poly(D,Llactide- co-glycolide) membranes. Biomed Mater Res 2004;70A:28-38.
102. Zare EN, Lakouraj MM, Mohseni M. Biodegradable polypyrrole/dextrin conductive nanocomposite: synthesis, characterization, antioxidant and antibacterial activity. Synth Met 2014;187:9-16.
103. Khor E, Li HC, Wee A. In situ polymerization of pyrrole in animal tissue in the formation of hybrid biomaterials. Biomaterials 1995;16:657-61.
104. Khor E, Li HC, Wee A. Animal tissue-polypyrrole hybrid biomaterials: shrinkage temperature evaluation. Biomaterials 1996;17:1877-9.
105. Chen S et al. PEDOT/MWCNT composite film coated microelectrode arrays for neural interface improvement. Sens Actuator A 2013;193:141-8.
106. Luo X, Weaver CL, Zhou DD, Greenberg R, Cui XT. Highly stable carbon nanotube doped poly(3,4-ethylenedioxythiophene) for chronic neural stimulation. Biomaterials 2011;32:5551-7.
107. Aznar-Cervantes S, Roca MI, Martinez JG, Meseguer-Olmo L, Cenis JL, Moraleda JM, et al. Fabrication of conductive electrospun silk fibroin scaffolds by coating with polypyrrole for biomedical applications. Bioelectrochemistry 2012;85:36-43.
108. Ku SH, Lee SH, Park CB. Synergic effects of nanofiber alignment and electroactivity on myoblast differentiation. Biomaterials 2012;33:6098-104.
109. Jeong SI, Jun ID, Choi MJ, Nho YC, Lee YM, Shin H. Development of electroactive and elastic nanofibers that contain polyaniline and poly(Llactide- co-e-caprolactone) for the control of cell adhesion. Macromol Biosci 2008;8:627-37.
110. Chen MC, Sun YC, Chen YH. Electrically conductive nanofibers with highly oriented structures and their potential application in skeletal muscle tissue engineering. Acta Biomater 2013;9:5562-72.
111. Small CJ, Too CO, Wallace GG. Responsive conducting polymer-hydrogel composites. Polym Gels Netw 1997;5:251-65.
112. Justin G, Guiseppi-Elie A. Electroconductive blends of poly(HEMA-co- PEGMA-co-HMMAco- SPMA) and poly(Py-co-PyBA): in vitro biocompatibility. J Bioact Compat Pol 2010;25:121-40.
113. Zhang Q, Yan Y, Li S, Feng T. The synthesis and characterization of a novel biodegradable and electroactive polyphosphazene for nerve regeneration. Mater Sci Eng C 2010;30:160-6.
114. Huang L et al. Synthesis and characterization of electroactive and biodegradable ABA block copolymer of polylactide and aniline pentamer. Biomaterials 2007;28:1741-51.
115. Cui X, Lee VA, Raphael Y, Wiler JA, Hetke JF, Anderson DJ, et al. Surface modification of neural recording electrodes with conducting polymer/ biomolecule blends. Biomed Mater Res 2001;56:261-72.
116. Williams RL, Doherty PJ. A preliminary assessment of poly(pyrrole) in nerve guide studies. J Mater Sci Mater Med 1994;5:429-33.
117. Wang X et al. Evaluation of biocompatibility of polypyrrole in vitro and in vivo. J Biomed Mater Res 2004;68A:411-22.
118. Richardson RT et al. The effect of polypyrrole with incorporated neurotrophin-3 on the promotion of neurite outgrowth from auditory neurons. Biomaterials 2007;28:513-23.
119. Jakubiec B et al. In vitro cellular response to polypyrrole-coated woven polyester fabrics: potential benefits of electrical conductivity. J Biomed Mater Res 1998;41:519-26.
120. Kim S, Oh WK, Jeong YS, Hong JY, Cho BR, Hahn JS, et al. Cytotoxicity of, and innate immune response to, size-controlled polypyrrole nanoparticles in mammalian cells. Biomaterials 2011;32:2342-50.
121. Kamalesh S, Tan P, Wang J, Lee T, Kang ET, Wang CH. Biocompatibility of electroactive polymers in tissues. J Biomed Mater Res 2000;52:467-78.
122. Bolin MH, Svennersten K, Wang X, Chronakis IS, Richter-Dahlfors A, Jager EWH, et al. Nano-fiber scaffold electrodes based on PEDOT for cell stimulation. Sens Actuator B 2009;142:451-6.
123. Karagkiozaki V, Karagiannidis PG, Gioti M, Kavatzikidou P, Georgiou D, Georgaraki E, et al. Bioelectronics meets nanomedicine for cardiovascular implants: PEDOT-based nanocoatings for tissue regeneration. Biochim Biophys Acta 2013;1830:4294-304.
124. Luo SC, Ali EM, Tansil NC, Yu HH, Gao S, Kantchev EAB, et al. Poly(3,4- ethylenedioxythiophene) (PEDOT) nanobiointerfaces: thin, ultrasmooth, and functionalized PEDOT films with in vitro and in vivo biocompatibility. Langmuir 2008;24:8071-7.
125. Zhou H, Cheng X, Rao L, Li T, Duan YY. Poly(3,4-ethylenedioxythiophene)/ multiwall carbon nanotube composite coatings for improving the stability of microelectrodes in neural prostheses applications. Acta Biomater 2013;9:6439-49.
126. Abidian MR, Ludwig KA, Marzullo TC, Martin DC, Kipke DR. Interfacing conducting polymer nanotubes with the central nervous system: chronic neural recording using poly(3,4-ethylenedioxythiophene) nanotubes. Adv Mater 2009;21:3764-70.
127. Ahuja T, Mir IA, Kumar D, Rajesh. Biomolecular immobilization on conducting polymers for biosensing applications. Biomaterials 2007;28:791-805.
128. Arora K et al. Application of electrochemically prepared polypyrrole- polyvinyl sulphonate films to DNA biosensor. Biosens Bioelectron 2006;21:1777-83.
129. Cosnier S. Biomolecule immobilization on electrode surfaces by entrapment or attachment to electrochemically polymerized films. A review. Biosens Bioelectron 1999;14:443-56.
130. Genies EM, Marchesiello M. Conducting polymers for biosensors, application to new glucose sensors GOD entrapped into polypyrrole, GOD adsorbed on poly(3-methylthiophene). Synth Met 1993;55-57:3677-82.
131. Prabhakar N, Arora K, Singh SP, Singh H, Malhotra BD. DNA entrapped polypyrrole-polyvinyl sulfonate film for application to electrochemical biosensor. Anal Biochem 2007;366:71-9.
132. Nien PC, Tung TS, Hoa KC. Amperometric glucose biosensor based on entrapment of glucose oxidase in a poly(3,4-ethylenedioxythiophene) film. Electroanalysis 2006;18:1408-15.
133. Wang J, Myung NV, Yun M, Monbouquette HG. Glucose oxidase entrapped in polypyrrole on high-surface-area Pt electrodes: a model platform for sensitive electroenzymatic biosensors. J Electroanal Chem 2005;575:139-46.
134. Jha SK, Kanungo M, Nath A, D'Souza SF. Entrapment of live microbial cells in electropolymerized polyaniline and their use as urea biosensor. Biosens Bioelectron 2009;24:2637-42.
135. Collazos-Castro JE, Polo JL, Hernández-Labrado GR, Padial-Cañete V, García- Rama C. Bioelectrochemical control of neural cell development on conducting polymers. Biomaterials 2010;31:9244-55.
136. De Giglio E, Sabbatini L, Zambonin PG. Development and analytical characterization of cysteine-grafted polypyrrole films electrosynthesized on Pt and Ti-substrates as precursors of bioactive interfaces. Biomater Sci Polym Ed 1999;10:845-58.
137. De Giglio E, Sabbatini L, Colucci S, Zambonin G. Synthesis, analytical characterization, and osteoblast adhesion properties on RGD-grafted polypyrrole coatings on titanium substrates. J Biomater Sci Polym Ed 2000;11:1073-83.
138. Bax DV et al. Cell patterning via linker-free protein functionalization of an organic conducting polymer (polypyrrole) electrode. Acta Biomater 2012;8:2538-48.
139. Cen L, Neoh KG, Li Y, Kang ET. Assessment of in vitro bioactivity of hyaluronic acid and sulfated hyaluronic acid functionalized electroactive polymer. Biomacromolecules 2004;5:2238-46.
140. Thompson BC, Richardson RT, Moulton SE, Evans AJ, O'Leary S, Clark GM, et al. Conducting polymers, dual neurotrophins and pulsed electrical stimulation - dramatic effects on neurite outgrowth. J Control Release 2010;141:161-7.
141. Wadhwa R, Lagenaur CF, Cui XT. Electrochemically controlled release of dexamethasone from conducting polymer polypyrrole coated electrode. J Control Release 2006;110:531-41.
142. Li Y, Neoh KG, Kang ET. Controlled release of heparin from polypyrrole- poly(vinyl alcohol) assembly by electrical stimulation. J Biomed Mater Res 2005;73A:171-81.
143. Stauffer WR, Cui XT. Polypyrrole doped with 2 peptide sequences from laminin. Biomaterials 2006;27:2405-13.
144. Zhang L, Stauffer WR, Jane EP, Sammak PJ, Cui XT. Enhanced differentiation of embryonic and neural stem cells to neuronal fates on laminin peptides doped polypyrrole. Macromol Biosci 2010;10:1456-64.
145. Guo B, Glavas L, Albertsson AC. Biodegradable and electrically conducting polymers for biomedical applications. Prog Polym Sci 2013;38:1263-86.
146. Shi G, Rouabhia M, Meng S, Zhang Z. Electrical stimulation enhances viability of human cutaneous fibroblasts on conductive biodegradable substrates. J Biomed Mater Res 2008;84A:1026-37.
147. Shi G, Zhang Z, Rouabhia M. The regulation of cell functions electrically using biodegradable polypyrrole-polylactide conductors. Biomaterials 2008;29:3792-8.
148. Zelikin AN, Lynn DM, Farhadi J, Martin I, Shastri V, Langer R. Erodible conducting polymers for potential biomedical applications. Angew Chem Int Ed 2002;41:141-4.
149. Massoumi B, Entezami AA. Electrochemically stimulated 2-ethylhexyl phosphate (EHP) release through redox switching of conducting polypyrrole film and polypyrrole/poly(N-methylpyrrole) or self-doped polyaniline bilayers. Polym Int 2002;51:555-60.
150. Miller LL, Zhou XU. Poly(N-methylpyrrolylium) poly(styrenesu1fonate). A conductive, electrically switchable cation exchanger that cathodically binds and anodically releases dopamine. Macromolecules 1987;20:1594-7.
151. Kontturi K, Pentti P, Sundholm G. Polypyrrole as a model membrane for drug delivery. J Electroanal Chem 1998;453:231-8.
152. Liu X, Yue Z, Higgins MJ, Wallace GG. Conducting polymers with immobilised fibrillar collagen for enhanced neural interfacing. Biomaterials 2011;32:7309-17.
153. Xu H et al. Conductive PPY/PDLLA conduit for peripheral nerve regeneration. Biomaterials 2014;35:225-35.
154. Weng B, Liu X, Shepherd R, Wallace GG. Inkjet printed polypyrrole/collagen scaffold: a combination of spatial control and electrical stimulation of PC12 cells. Synth Met 2012;162:1375-80.
155. Huang J, Hu X, Lu L, Ye Z, Zhang Q, Luo Z. Electrical regulation of Schwann cells using conductive polypyrrole/chitosan polymers. J Biomed Mater Res 2010;93A:164-74.
156. Hsiao CW et al. Electrical coupling of isolated cardiomyocyte clusters grown on aligned conductive nanofibrous meshes for their synchronized beating. Biomaterials 2013;34:1063-72.
157. Gandhi MR, Murray P, Spinks GM, Wallace GG. Mechanism of electromechanical actuation in polypyrrole. Synth Met 1995;73:247-56.
158. Kaneto K, Kaneko M, Min Y, MacDiarmid AG. "Artificial muscle": electromechanical actuators usingpolyanilinefilms. SynthMet 1995;71:2211-2.
159. Madden JD, Cush RA, Kanigan TS, Hunter IW. Fast contracting polypyrrole actuators. Synth Met 2000;113:185-92.
160. Okuzaki H, Suzuki H, Ito T. Electrically driven PEDOT/PSS actuators. Synth Met 2009;159:2233-6.
161. Bay L, Jacobsen T, Skaarup S. Mechanism of actuation in conducting polymers: osmotic expansion. J Phys Chem B 2001;105:8492-7.
162. Smela E, Gadegaard N. Surprising volume change in PPy(DBS): an atomic force microscopy study. Adv Mater 1999;11:953-7.
163. Jager EWH. Conducting polymer actuators for medical devices and cell mechanotransduction. In: IEEE/ASME international conference on advanced intelligent, mechatronics; 2013. p. 1661-6.
164. Chiu LLY, Radisic M. Cardiac tissue engineering. Curr Opin Chem Eng 2013;2:41-52.
165. Subramony SD, Dargis BR, Castillo M, Azeloglu EU, Tracey MS, Su A, et al. The guidance of stem cell differentiation by substrate alignment and mechanical stimulation. Biomaterials 2013;34:1942-53.
166. Svennersten K, Berggren M, Richter-Dahlfors A, Jager EWH. Mechanical stimulation of epithelial cells using polypyrrole microactuators. Lab Chip 2011;11:3287.
167. Demer LL, Wortham CM, Dirksen ER, Sanderson MJ. Mechanical stimulation induces intercellular calcium signalling in bovine aortic endothelial cells. Am J Physiol-Heart C 1993;264:H2094-102.
168. Jager EWH, Bolin MH, Svennersten K, Wang X, Richter-Dahlfors A, Berggren M. Electroactive surfaces based on conducting polymers for controlling cell adhesion, signalling, and proliferation. In: International solid-state sensors, actuators and microsystems conference; 2009. p. 1778-81.
169. Hu J et al. Electroactive aniline pentamer cross-linking chitosan for stimulation growth of electrically sensitive cells. Biomacromolecules 2008;9:2637-44.
170. Gizdavic-Nikolaidis M, Ray S, Bennett J, Swift S, Bowmaker G, Easteal A. Electrospun poly(aniline-co-ethyl 3-aminobenzoate)/poly(lactic acid) nanofibers and their potential in biomedical applications. J Polym Sci Part A: Polym Chem 2011;49:4902-10.
171. Gizdavic-Nikolaidis M, Ray S, Bennett JR, Easteal AJ, Cooney RP. Electrospun functionalized polyaniline copolymer-based nanofibers with potential application in tissue engineering. Macromol Biosci 2010;10:1424-31.
172. Kumar D, Sharma RC. Advances in conductive polymers. Eur Polym J 1998;34:1053-60.
173. Wan M. Introduction of conducting polymers. In: Wan M, editor. Conducting polymers with micro or nanometer structure. Berlin: Springer; 2008. p. 1-15.
174. Epstein AJ. Electrical conductivity in conjugated polymers. In: Rupprecht L, editor. Conductive polymers and plastics in industrial applications. Norwich, NY: William Andrew Publishing/Plastics Design Library; 1999. p. 1-9.
175. Kirchmeyer S, Reuter K. Scientific importance, properties and growing applications of poly(3,4-ethylenedioxythiophene). J Mater Chem 2005;15:2077-88.
176. Ribo JM, Acero C, Anglada MC, Dicko A, Tura JM, Ferrer-Anglada N, et al. On the structure and transport properties of polypyrroles. Butll Soc Cat Cien 1992;13:335-51.
177. Street GB, Lindsey SE, Nazzal AI, Wynne KJ. The structure and mechanical properties of polypyrrole. Mol Cryst Liq Cryst 1985;118:137-48.
178. MacDiarmid AG, Epstein AJ. Secondary doping in polyaniline. Synth Met 1995;69:85-92.
179. MacDiarmid AG, Chiang JC, Richter AF. Polyaniline: a new concept in conducting polymers. Synth Met 1987;18:285-90.
180. Pouget JP, Jdzefowiczt ME, Epstein AJ, Tang X, MacDiarmid AG. X-ray structure of polyaniline. Macromolecules 1991;24:779-89.
181. Tourillon G, Garnier F. Morphology and crystallographic, structure of polythiophene and derivatives. Mol Cryst Liq Cryst 1985;118:221-6.
182. Batz P, Schmeisser D, Gopel W. Electronic structure of polypyrrole films. Phys Rev B 1991;43:9178-89.
183. Aasmundtveit KE, Samuelsent EJ, Pettersson LAA, Inganas O, Johansson T, Feidenhans R. Structure of thin films of poly(3,4-ethylenedioxythiophene. Synth Met 1999;101:561-4.