Peripheral nerve regeneration strategies: Electrically stimulating polymer based nerve growth conduits

Critical Reviews in Biomedical Engineering

Volumn 43, Issue 2-3, 2015, Pages 131-149

  Anderson, Matthew ^a   Shelke, Namdev B ^a   Manoukian, Ohan S ^b   Yu, Xiaojun ^c   McCullough, Louise D ^a   Kumbar, Sangamesh G ^a,b  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b University of Connecticut   (United States)

^c Stevens Institute of Technology   (United States)

Author keywords

Electrical stimulation; Electrically conducting polymers; Nerve growth conduit; Peripheral nerve regeneration; Tissue engineering

Indexed keywords

BIOCOMPATIBILITY; CELL ADHESION; CELLS; CONDUCTING POLYMERS; MOLECULAR BIOLOGY; TISSUE; TISSUE ENGINEERING;

CELLULAR ACTIVITIES; COMBINATORIAL DEVICES; ELECTRICAL STIMULATIONS; ELECTRICALLY CONDUCTING POLYMER; ELECTRICALLY CONDUCTIVE POLYMERS; NERVE GROWTH CONDUIT; PERIPHERAL NERVE REGENERATION; TISSUE ENGINEERED NERVE GRAFTS;

TISSUE REGENERATION;

POLY(3,4 ETHYLENEDIOXYTHIOPHENE); POLYANILINE; POLYMER; POLYPYRROLE; UNCLASSIFIED DRUG; BIOMATERIAL;

ARTICLE; BIOCOMPATIBILITY; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CHEMICAL STRUCTURE; ELECTROSTIMULATION; NERVE FIBER GROWTH; NERVE GRAFT; NERVE GROWTH CONDUIT; NERVE REGENERATION; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; SCHWANN CELL; TISSUE ENGINEERING; TISSUE REGENERATION; ELECTRIC CONDUCTIVITY; ELECTROTHERAPY; HUMAN; PERIPHERAL NERVE; PHYSIOLOGY; PROCEDURES;

BIOCOMPATIBLE MATERIALS; ELECTRIC CONDUCTIVITY; ELECTRIC STIMULATION THERAPY; GUIDED TISSUE REGENERATION; HUMANS; NERVE REGENERATION; PERIPHERAL NERVES; POLYMERS; TISSUE ENGINEERING;

EID: 84960380430     PISSN: 0278940X     EISSN: 1943619X     Source Type: Journal    
DOI: 10.1615/critrevbiomedeng.2015014015     Document Type: Article

References (171)

1. Taylor CA, Braza D, Rice JB, Dillingham T. The incidence of peripheral nerve injury in extremity trauma. Am J Phys Med Rehabil. 2008;87(5):381-5.
2. Grinsell D, Keating C. Peripheral nerve reconstruction after injury: A review of clinical and experimental therapies. Biomed Res Int. 2014;2014:1-13.
3. Arslantunali D, Dursun T, Yucel D, Hasirci N, Hasirci V. Peripheral nerve conduits: Technology update. Med Devices (Auckland, NZ). 2014;7:405-24.
4. Krebs C, Weinberg J, Akeeson. Lippincott's Illustrated Reviews: Neuroscience. Baltimore (MD): Lippincott Williams & Wilkins, 2012.
5. Pfister LA, Papaloïzos M, Merkle HP, Gander B. Nerve conduits and growth factor delivery in peripheral nerve repair. J Peripher Nerv Syst. 2007;12(2):65-82.
6. Konofaos P, Ver Halen JP. Nerve repair by means of tubulization: Past, present, future. J Reconstr Microsurg. 2013;29(3):149-64.
7. Williams LR, Longo FM, Powell HC, Lundborg G, Varon S. Spatial-temporal progress of peripheral nerve regeneration within a silicone chamber: Parameters for a bioassay. J Compar Neurol. 1983;218(4):460-70.
8. Belkas JS, Shoichet MS, Midha R. Peripheral nerve regeneration through guidance tubes. Neurol Res. 2004;26(2):151-60.
9. Chong JK. Nerve regeneration through preformed pseudosynovial tubes. Plast Reconstr Surg. 1980;66(6):866.
10. Seckel BR, Chiu TH, Sidman RL. Nerve regeneration through synthetic biodegradable nerve guides: Regulation by the target organ. Plast Reconstr Surg. 1984;74(2):173-81.
11. Johnson EO, Soucacos PN. Nerve repair: Experimental and clinical evaluation of biodegradable artificial nerve guides. Injury. 2008;39(3):30-36.
12. Rich KM, Alexander TD, Pryor JC, Hollowell JP. Nerve growth factor enhances regeneration through silicone chambers. Exp Neurol. 1989;105(2):162-70.
13. Runge MB, Dadsetan M, Baltrusaitis J, Ruesink T, Lu L, Windebank AJ, Yaszemski MJ. Development of electrically conductive oligo (polyethylene glycol) fumarate-polypyrrole hydrogels for nerve regeneration. Biomacromolecules. 2010;11(11):2845-53.
14. Lee JY, Bashur CA, Milroy CA, Forciniti L, Goldstein AS, Schmidt CE. Nerve growth factor-immobilized electrically conducting fibrous scaffolds for potential use in neural engineering applications. IEEE Trans Nanobiosci. 2012;11(1):15-21.
15. Xu H, Holzwarth JM, Yan Y, Xu P, Zheng H, Yin Y, Li S, Ma PX. Conductive PPY/PDLLA conduit for peripheral nerve regeneration. Biomaterials. 2014;35(1):225-35.
16. Durgam H, Sapp S, Deister C, Khaing Z, Chang E, Luebben S, Schmidt CE. Novel degradable co-polymers of polypyrrole support cell proliferation and enhance neurite out-growth with electrical stimulation. J Biomater Sci Polym Ed. 2010;21(10):1265-82.
17. Kotwal A, Schmidt CE. Electrical stimulation alters protein adsorption and nerve cell interactions with electrically conducting biomaterials. Biomaterials. 2001;22(10):1055-64.
18. Zeng J, Huang Z, Yin G, Qin J, Chen X, Gu J. Fabrication of conductive NGF-conjugated polypyrrole-poly(l-lactic acid) fibers and their effect on neurite outgrowth. Colloids Surf B. 2013;110:450-57.
19. Runge MB, Dadsetan M, Baltrusaitis J, Knight AM, Ruesink T, Lazcano EA, Lu L, Windebank AJ, Yaszemski MJ. The development of electrically conductive polycaprolactone fumarate-polypyrrole composite materials for nerve regeneration. Biomaterials. 2010;31(23):5916-26.
20. Quigley AF, Razal JM, Thompson BC, Moulton SE, Kita M, Kennedy EL, Clark GM, Wallace GG, Kapsa RM. A Conducting-polymer platform with biodegradable fibers for stimulation and guidance of axonal growth. Adv Mater. 2009;21(43):4393-97.
21. Chen Y-S. Effects of electrical stimulation on peripheral nerve regeneration. BioMedicine. 2011;1(1):33-36.
22. Williams D. Benefit and risk in tissue engineering. Mater Today. 2004;7(5):24-29.
23. Shelke NB, James R, Laurencin CT, Kumbar SG. Polysaccharide biomaterials for drug delivery and regenerative engineering. Polym Adv Technol. 2014;25(5):448-60.
24. Tamaki T. Bridging long gap peripheral nerve injury using skeletal muscle-derived multipotent stem cells. Neural Regener Res. 2014;9(14):1333-36.
25. Zhang P, Lu X, Chen J, Chen Z. Schwann cells originating from skin-derived precursors promote peripheral nerve regeneration in rats. Neural Regener Res. 2014;9(18):1696-702.
26. Ma S, Peng C, Wu S, Wu D, Gao C. Sciatic nerve regeneration using a nerve growth factor-containing fibrin glue membrane. Neural Regener Res. 2013;8(36):3416-22.
27. Kapur TA, Shoichet MS. Chemically-bound nerve growth factor for neural tissue engineering applications. J Biomater Sci Polym Ed. 2003;14(4):383-94.
28. 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.
29. Kim Y-T, Haftel VK, Kumar S, Bellamkonda RV. The role of aligned polymer fiber-based constructs in the bridging of long peripheral nerve gaps. Biomaterials. 2008;29(21):3117-27.
30. Calvey C, Zhou W, Stakleff KS, Sendelbach-Sloan P, Harkins AB, Lanzinger W, Willits RK. Short-term electrical stimulation to promote nerve repair and functional recovery in a rat model. J Hand Surg Am. 2014;40(2):314-22.
31. Ghasemi-Mobarakeh L, Prabhakaran MP, Morshed M, Nasr-Esfahani MH, Baharvand H, Kiani S, Al-Deyab SS, Ramakrishna S. Application of conductive polymers, scaffolds and electrical stimulation for nerve tissue engineering. J Tissue Engin Regen Med. 2011;5(4):e17-e35.
32. Prasad Shastri V, Lendlein A. Engineering materials for regenerative medicine. MRS Bull. 2010;35(08):571-77.
33. Shastri VR, Schmidt CE, Kim T-H, Vacanti JP, Langer R. Polypyrrole-a potential candidate for stimulated nerve regeneration. MRS Online Proceedings Library. 1995;414.
34. Lin MY, Manzano G, Gupta R. Nerve allografts and conduits in peripheral nerve repair. Hand Clin. 2013;29(3):331-48.
35. Shelke NB, Anderson M, Idrees SM, Nip J, Nip, Donde S, Gronowicz G, Kumbar SG. Polyester nano- and micro-technologies for tissue engineering. In: Ravikumar MNV, ed. Handbook of Polyester Drug Delivery Systems. Singapore: Pan Stanford Publishing, 2015.
36. James R, Toti US, Laurencin CT, Kumbar SG. Electrospun nanofibrous scaffolds for engineering soft connective tissues. Biomedical nanotechnology. New York (NY): Springer; 2011. p. 243-58.
37. Lee J-W, Serna F, Schmidt CE. Carboxy-endcapped conductive polypyrrole: Biomimetic conducting polymer for cell scaffolds and electrodes. Langmuir. 2006;22(24):9816-9.
38. Haan N, Song B. Therapeutic application of electric fields in the injured nervous system. Adv Wound Care (New Rochelle). 2014;3(2):156-65.
39. Salmons S, Ashley Z, Sutherland H, Russold MF, Li F, Jarvis JC. Functional electrical stimulation of denervated muscles: Basic issues. Artif Organs. 2005;29(3): 199-202.
40. Akai M, Hayashi K. Effect of electrical stimulation on musculoskeletal systems; a meta-analysis of controlled clinical trials. Bioelectromagnetics. 2002;23(2):132-43.
41. Aaron RK, Ciombor DM. Therapeutic effects of electromagnetic fields in the stimulation of connective tissue repair. J Cell Biochem. 1993;52(1):42-6.
42. Williams HB. The value of continuous electrical muscle stimulation using a completely implantable system in the preservation of muscle function following motor nerve injury and repair: An experimental study. Microsurgery. 1996;17(11):589-96.
43. Hampton S, King L. Healing an intractable wound using bio-electrical stimulation therapy. Br J Nurs. 2005;14(15):S30-2.
44. Araújo R, Franciulli P, Assis R, Souza R, Mochizuki L. Effects of laser, ultrasound and electrical stimulation on the repair of achilles tendon injuries in rats: A comparative study. Braz J Morphol Sci. 2007;24(3):187-91.
45. Mercóla JM, Kirsch D. The basis for micro current electrical therapy in conventional medical practice. J Advancement Med. 1995;8(2):107-20.
46. Stanish W, Rubinovich M, Kozey J, MacGillvary G. The use of electricity in ligament and tendon repair. Physician Sports Med. 1985;13:108-16.
47. Stanish WD, Lai A. New concepts of rehabilitation following anterior cruciate reconstruction. Clin Sports Med. 1993;12(1):25-58.
48. Hang J, Kong L, Gu JW, Adair TH. VEGF gene expression is upregulated in electrically stimulated rat skeletal muscle. Am J Physiol. 1995;269(5 Pt 2):H1827-31.
49. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, Wagner PD. Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol. 1996;81(1):355-61.
50. Kanno S, Oda N, Abe M, Saito S, Hori K, Handa Y, Tabayashi K, Sato Y. Establishment of a simple and practical procedure applicable to therapeutic angiogenesis. Circulation. 1999;99(20):2682-7.
51. Annex BH, Torgan CE, Lin P, Taylor DA, Thompson MA, Peters KG, Kraus WE. Induction and maintenance of increased VEGF protein by chronic motor nerve stimulation in skeletal muscle. Am J Physiol. 1998;274(3 Pt 2): H860-7.
52. Dawson JM, Hudlicka O. Can changes in microcirculation explain capillary growth in skeletal muscle? Int J Exp Pathol. 1993;74(1):65-71.
53. Gavin TP, Spector DA, Wagner H, Breen EC, Wagner PD. Nitric oxide synthase inhibition attenuates the skeletal muscle VEGF mRNA response to exercise. J Appl Physiol. 2000;88(4):1192-8.
54. Hudlicka O, Brown MD, Silgram H. Inhibition of capillary growth in chronically stimulated rat muscles by N(G)- nitro-l-arginine, nitric oxide synthase inhibitor. Microvasc Res. 2000;59(1):45-51.
55. Machado AFP, Santana EF, Tacani PM, Liebano RE. The effects of transcutaneous electrical nerve stimulation on tissue repair: A literature review. Can J Plast Surg. 2012;20(4):237.
56. Haddad JB, Obolensky AG, Shinnick P. The biologic effects and the therapeutic mechanism of action of electric and electromagnetic field stimulation on bone and cartilage: New findings and a review of earlier work. J Altern Complement Med. 2007;13(5):485-90.
57. Sirivisoot S, Pareta R, Harrison BS. Protocol and cell responses in three-dimensional conductive collagen gel scaffolds with conductive polymer nanofibres for tissue regeneration. Interface Focus. 2014;4(1):20130050.
58. Pires F, Ferreira Q, Rodrigues CA, Morgado J, Ferreira FC. Neural stem cell differentiation by electrical stimulation using a cross-linked PEDOT substrate: Expanding the use of biocompatible conjugated conductive polymers for neural tissue engineering. Biochimica Biophysica Acta (BBA)-General Subjects. 2015;1850(6): 1158-68.
59. Min Y, Liu Y, Poojari Y, Wu J-C, Hildreth Iii BE, Rosol TJ, Epstein AJ. Self-doped polyaniline-based interdigitated electrodes for electrical stimulation of osteoblast cell lines. Synthetic Metals. 2014;198(0):308-13.
60. Rajzer I, Rom M, Menaszek E, Pasierb P. Conductive PANI patterns on electrospun PCL/gelatin scaffolds modified with bioactive particles for bone tissue engineering. Mater Lett. 2015;138(0):60-63.
61. Qazi TH, Rai R, Dippold D, Roether JE, Schubert DW, Rosellini E, Barbani N, Boccaccini AR. Development and characterization of novel electrically conductive PANI-PGS composites for cardiac tissue engineering applications. Acta Biomater. 2014;10(6):2434-45.
62. Moura RM, de Queiroz AAA. Dendronized polyaniline nanotubes for cardiac tissue engineering. Artif Org. 2011;35(5):471-77.
63. Borriello A, Guarino V, Schiavo L, Alvarez-Perez M, Ambrosio L. Optimizing PANi doped electroactive substrates as patches for the regeneration of cardiac muscle. J Mater Sci Mater Med. 2011;22(4):1053-62.
64. 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(5):501-7.
65. Zhang J, Qiu K, Sun B, Fang J, Zhang K, Hany E-H, Al-Deyab SS, Mo X. The aligned core-sheath nanofibers with electrical conductivity for neural tissue engineering. J Mater Chem B. 2014;2:7945-54.
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(11):3605-19.
67. James R, Nagarale RK, Sachan VK, Badalucco C, Bhattacharya PK, Kumbar SG. Synthesis and characterization of electrically conducting polymers for regenerative engineering applications: Sulfonated ionic membranes. Polym Advan Technol. 2014;25(12):1439-45.
68. Balint R, Cassidy NJ, Cartmell SH. Conductive polymers: Towards a smart biomaterial for tissue engineering. Acta Biomater. 2014;10(6):2341-53.
69. Shiga T. Deformation and viscoelastic behavior of polymer gels in electric fields. Neutron Spin Echo Spectroscopy Viscoelasticity Rheology. Vol. 134. Berlin: Springer; 1997. p. 131-63.
70. Pei Q, Inganläs O. Conjugated polymers and the bending cantilever method: Electrical muscles and smart devices. Adv Mater. 1992;4(4):277-78.
71. Schmidt CE, Leach JB. Neural tissue engineering: Strategies for repair and regeneration. Annu Rev Biomed Eng. 2003;5:293-347.
72. Zhang N, Yan H, Wen X. Tissue-engineering approaches for axonal guidance. Brain Res Brain Res Rev. 2005;49(1): 48-64.
73. de Ruiter GC, Malessy MJ, Yaszemski MJ, Windebank AJ, Spinner RJ. Designing ideal conduits for peripheral nerve repair. Neurosurg Focus. 2009;26(2):E5.
74. Moroder P, Runge MB, Wang H, Ruesink T, Lu L, Spinner RJ, Windebank AJ, Yaszemski MJ. Material properties and electrical stimulation regimens of polycaprolactone fumarate-polypyrrole scaffolds as potential conductive nerve conduits. Acta Biomater. 2011;7(3):944-53.
75. Huang J, Ye Z, Hu X, Lu L, Luo Z. Electrical stimulation induces calcium-dependent release of NGF from cultured Schwann cells. Glia. 2010;58(5):622-31.
76. Luo B, Huang J, Lu L, Hu X, Luo Z, Li M. Electrically induced brain-derived neurotrophic factor release from schwann cells. J Neurosci Res. 2014;92(7):893-903.
77. 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 Part A. 2010;93(1): 164-74.
78. Lee AC, Vivian MY, Lowe JB, Brenner MJ, Hunter DA, Mackinnon SE, Sakiyama-Elbert SE. Controlled release of nerve growth factor enhances sciatic nerve regeneration. Exp Neurol. 2003;184(1):295-303.
79. Terris DJ, Toft KM, Moir M, Lum J, Wang M. Brain-derived neurotrophic factor-enriched collagen tubule as a substitute for autologous nerve grafts. Arch Otolaryngol Head Neck Surg. 2001;127(3):294-98.
80. Mohanna P-N, Terenghi G, Wiberg M. Composite PHB-GGF conduit for long nerve gap repair: A long-term evaluation. Scand J Plast Reconstr Surg Hand Surg. 2005;39(3):129-37.
81. Xu X, Yu H, Gao S, Mao H-Q, Leong KW, Wang S. Poly-phosphoester microspheres for sustained release of biologically active nerve growth factor. Biomaterials. 2002;23(17):3765-72.
82. Ziv-Polat O, Shahar A, Levy I, Skaat H, Neuman S, Fregnan F, Geuna S, Grothe C, Haastert-Talini K, Margel S. The role of neurotrophic factors conjugated to iron oxide nanoparticles in peripheral nerve regeneration: In vitro studies. Biomed Res Int. 2014;2014:267808.
83. Zhang S, Uludağ H. Nanoparticulate systems for growth factor delivery. Pharm Res. 2009;26(7):1561-80.
84. Schlosshauer B, Müller E, Schröder B, Planck H, Müller H-W. Rat Schwann cells in bioresorbable nerve guides to promote and accelerate axonal regeneration. Brain Res. 2003;963(1):321-26.
85. Armstrong SJ, Wiberg M, Terenghi G, Kingham PJ. ECM molecules mediate both Schwann cell proliferation and activation to enhance neurite outgrowth. Tissue Eng. 2007;13(12):2863-70.
86. Bell JH, Haycock JW. Next generation nerve guides: Materials, fabrication, growth factors, and cell delivery. Tissue Eng Part B. 2012;18(2):116-28.
87. Lopes FRP, de Moura Campos LC, Corrêa JD, Balduino A, Lora S, Langone F, Borojevic R, Martinez AMB. Bone marrow stromal cells and resorbable collagen guidance tubes enhance sciatic nerve regeneration in mice. Exp Neurol. 2006;198(2):457-68.
88. di Summa PG, Kalbermatten DF, Pralong E, Raffoul W, Kingham PJ, Terenghi G. Long-term in vivo regeneration of peripheral nerves through bioengineered nerve grafts. Neuroscience. 2011;181:278-91.
89. Santiago LY, Clavijo-Alvarez J, Brayfield C, Rubin JP, Marra KG. Delivery of adipose-derived precursor cells for peripheral nerve repair. Cell Transplant. 2009;18(2):145-58.
90. Thrivikraman G, Madras G, Basu B. Intermittent electrical stimuli for guidance of human mesenchymal stem cell lineage commitment towards neural-like cells on electroconductive substrates. Biomaterials. 2014;35(24): 6219-35.
91. Sun S, Titushkin I, Cho M. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus. Bioelectrochemistry. 2006;69(2):133-41.
92. Yamada E, Hashimoto S, Tachibana K, Okada M, Yamasaki K, Kondo H, Imoto K, Mochizuki S, Fujisato T, Ohsuga M, Effect of electric stimulation on adhesion and proliferation of cultured muscle cells. Proceedings of 12th World Multi-Conference on Systemics Cybernetics and Informatics. 2008.
93. Blank M. Protein and DNA reactions stimulated by electromagnetic fields. Electromagn Biol Med. 2008;27(1):3-23.
94. Feng JF, Liu J, Zhang XZ, Zhang L, Jiang JY, Nolta J, Zhao M. Guided migration of neural stem cells derived from human embryonic stem cells by an electric field. Stem Cells. 2012;30(2):349-55.
95. Jahanshahi A, Schönfeld L-M, Lemmens E, Hendrix S, Temel Y. In vitro and in vivo neuronal electrotaxis: A potential mechanism for restoration? Mol Neurobiol. 2014;49(2):1005-16.
96. Lu M-C, Tsai C-C, Chen S-C, Tsai F-J, Yao C-H, Chen Y-S. Use of electrical stimulation at different current levels to promote recovery after peripheral nerve injury in rats. J Trauma Acute Care Surg. 2009;67(5):1066-72.
97. Haastert-Talini K, Schmitte R, Korte N, Klode D, Ratzka A, Grothe C. Electrical stimulation accelerates axonal and functional peripheral nerve regeneration across long gaps. J Neurotrauma. 2011;28(4):661-74.
98. Yeh CC, Lin YC, Tsai FJ, Huang CY, Yao C-H, Chen Y-S. Timing of applying electrical stimulation is an important factor deciding the success rate and maturity of regenerating rat sciatic nerves. Neurorehabil Neural Repair. 2010;24(8):730-35.
99. Huang J, Zhang Y, Lu L, Hu X, Luo Z. Electrical stimulation accelerates nerve regeneration and functional recovery in delayed peripheral nerve injury in rats. Eur J Neurosci. 2013;38(12):3691-701.
100. Bakhshi A, Bhalla G. Electrically conducting polymers: Materials of the twentyfirst century. J Sci Indust Res. 2004;63:715-28.
101. Bredas JL, Street GB. Polarons, bipolarons, and solitons in conducting polymers. Acc Chem Res. 1985;18(10): 309-15.
102. Schmidt CE, Shastri VR, Vacanti JP, Langer R. Stimulation of neurite outgrowth using an electrically conducting polymer. Proc Natl Acad Sci U S A. 1997;94(17):8948-53.
103. Subramanian A, Krishnan UM, Sethuraman S. Develop-ment of biomaterial scaffold for nerve tissue engineering: Biomaterial mediated neural regeneration. J Biomed Sci. 2009;16(1):108.
104. Stewart E, Kobayashi NR, Higgins MJ, Quigley AF, Jamali S, Moulton SE, Kapsa RM, Wallace GG, Crook JM. Electrical stimulation using conductive polymer polypyrrole promotes differentiation of human neural stem cells: A biocompatible platform for translational neural tissue engineering. Tissue Eng Part C. 2014;21(4):385-93.
105. Cao J, Hu G, Peng Z, Du K, Cao Y. Polypyrrole-coated LiCoO2 nanocomposite with enhanced electrochemical properties at high voltage for lithium-ion batteries. J Power Sources. 2015;281(0):49-55.
106. Fan X, Yang Z, He N. Hierarchical nanostructured polypyrrole/graphene composites as supercapacitor electrode. RSC Adv. 2015;5(20):15096-102.
107. Chee W, Lim H, Harrison I, Chong K, Zainal Z, Ng C, Huang N. Performance of flexible and binderless polypyrrole/graphene oxide/zinc oxide supercapacitor electrode in a symmetrical two-electrode configuration. Electrochim Acta. 2015;157(0):88-94.
108. Zhang Y, Zhen Z, Zhang Z, Lao J, Wei J, Wang K, Kang F, Zhu H. In situ synthesis of carbon nanotube/ graphene composite sponge and its application as compressible supercapacitor electrode. Electrochim Acta. 2015;157(0):134-41.
109. Xu J, Wang D, Yuan Y, Wei W, Gu S, Liu R, Wang X, Liu L, Xu W. Polypyrrole-coated cotton fabrics for flexible supercapacitor electrodes prepared using CuO nanoparticles as template. Cellulose. 2015;22(2):1355-63.
110. Ayenimo JG, Adeloju SB. Inhibitive potentiometric detection of trace metals with ultrathin polypyrrole glucose oxidase biosensor. Talanta. 2015;137:62-70.
111. Seven B, Bourourou M, Elouarzaki K, Constant JF, Gondran C, Holzinger M, Cosnier S, Timur S. Impedimetric biosensor for cancer cell detection. Electrochem Commun. 2013;37:36-9.
112. Shamaeli E, Alizadeh N. Functionalized gold nanoparticle-polypyrrole nanobiocomposite with high effective surface area for electrochemical/pH dual stimuli-responsive smart release of insulin. Colloids Surf B. 2015;126:502-9.
113. Lee JY, Lee J-W, Schmidt CE. Neuroactive conducting scaffolds: Nerve growth factor conjugation on active ester-functionalized polypyrrole. J R Soc Interface. 2008;6(38):801-10.
114. Yu Q, Xu S, Zhang K, Shan Y. Multi-porous electroactive poly(L-lactic acid)/polypyrrole composite micro/nano fibrous scaffolds promote neurite outgrowth in PC12 cells. Neural Regen Res. 2013;8(1):31-8.
115. Nguyen HT, Sapp S, Wei C, Chow JK, Nguyen A, Coursen J, Luebben S, Chang E, Ross R, Schmidt CE. Electric field stimulation through a biodegradable polypyrrole-co-polycaprolactone substrate enhances neural cell growth. J Biomed Mater Res A. 2014;102(8):2554-64.
116. Meng S, Rouabhia M, Zhang Z. Electrical stimulation modulates osteoblast proliferation and bone protein production through heparin-bioactivated conductive scaffolds. Bioelectromagnetics. 2013;34(3):189-99.
117. Pelto J, Björninen M, Pälli A, Talvitie E, Hyttinen J, Mannerström B, Suuronen Seppanen R, Kellomäki M, Miettinen S, Haimi S. Novel polypyrrole-coated polylactide scaffolds enhance adipose stem cell proliferation and early osteogenic differentiation. Tissue Eng Part A. 2013;19(7-8):882-92.
118. Chu X-H, Xu Q, Feng Z-Q, Xiao J-Q, Li Q, Sun X-T, Cao Y, Ding Y-T. In vitro biocompatibility of polypyrrole/PLGA conductive nanofiber scaffold with cultured rat hepatocytes. Mater Res Exp. 2014;1(3):035402.
119. Ruhparwar A, Piontek P, Ungerer M, Ghodsizad A, Partovi S, Foroughi J, Szabo G, Farag M, Karck M, Spinks GM. Electrically contractile polymers augment right ventricular output in the heart. Artif Organs. 2014;38(12): 1034-9.
120. Efimov ON. Polypyrrole: A conducting polymer; its synthesis, properties and applications. Russian Chemical Reviews. 1997;66(5):443-57.
121. Wang X, Gu X, Yuan C, Chen S, Zhang P, Zhang T, Yao J, Chen F, Chen G. Evaluation of biocompatibility of polypyrrole in vitro and in vivo. J Biomed Mater Res A. 2004;68(3):411-22.
122. Forciniti L, Ybarra J 3rd, Zaman MH, Schmidt CE. Schwann cell response on polypyrrole substrates upon electrical stimulation. Acta Biomater. 2014;10(6):2423-33.
123. George PM, Saigal R, Lawlor MW, Moore MJ, LaVan DA, Marini RP, Selig M, Makhni M, Burdick JA, Langer R, Kohane DS. Three-dimensional conductive constructs for nerve regeneration. J Biomed Mater Res A. 2009;91(2):519-27.
124. Shi Z, Gao H, Feng J, Ding B, Cao X, Kuga S, Wang Y, Zhang L, Cai J. In situ synthesis of robust conductive cellulose/polypyrrole composite aerogels and their potential application in nerve regeneration. Angew Chem. 2014;126(21):5484-8.
125. Yunusa Z, Hamidon MN, Ismail A, Isa MM, Yaacob MH, Rahmanian S, Ibrahim SA, Shabaneh AA. Development of a hydrogen gas sensor using a double saw resonator system at room temperature. Sensors. 2015;15(3):4749-65.
126. Bai S, Sun C, Wan P, Wang C, Luo R, Li Y, Liu J, Sun X. Transparent conducting films of hierarchically nanostructured polyaniline networks on flexible substrates for high-performance gas sensors. Small. 2015;11(3): 306-10.
127. Chen D, Lei S, Chen Y. A single polyaniline nanofiber field effect transistor and its gas sensing mechanisms. Sensors. 2011;11(7):6509-16.
128. Lim JW, Haq AU, Kim SO, Direct growth of polyaniline chains from nitrogen site of N-doped carbon nanotubes for high performance supercapacitor. Adv Sci Technol. 2014;93:164-7.
129. Huang H, Gan M, Ma L, Yu L, Hu H, Yang F, Li Y, Ge C. Fabrication of polyaniline/graphene/titania nanotube arrays nanocomposite and their application in supercapacitors. J Alloys Compd. 2015;630(0):214-21.
130. Lee S-N, Baek S, Amaresh S, Aravindan V, Chung KY, Cho BW, Yoon W-S, Lee Y-S. Cu-Li2MnSiO4-polyaniline composite hybrids as high performance cathode for lithium batteries. J Alloy Compd. 2015;630(0):292-8.
131. Tang X, Tian M, Qu L, Zhu S, Guo X, Han G, Sun K, Hu X, Wang Y, Xu X. Functionalization of cotton fabric with graphene oxide nanosheet and polyaniline for conductive and UV blocking properties. Synt Met. 2015;202(0):82-8.
132. Baniasadi H, Ramazani SA, Mashayekhan S. Fabrication and Characterization of Conductive Chitosan/Gelatin-based Scaffolds for Nerve Tissue Engineering. Int J Biol Macromol. 2015;74(0):360-6.
133. Chen M-C, Sun Y-C, Chen Y-H. Electrically conductive nanofibers with highly oriented structures and their potential application in skeletal muscle tissue engineering. Acta Biomater. 2013;9(3):5562-72.
134. Guarino V, Alvarez-Perez MA, Borriello A, Napolitano T, Ambrosio L. Conductive PANi/PEGDA macroporous hydrogels for nerve regeneration. Adv Healthc Mater. 2013;2(1):218-27.
135. Barry FP, Murphy JM. Mesenchymal stem cells: Clinical applications and biological characterization. Int J Biochem Cell Biol. 2004;36(4):568-84.
136. Abdallah B, Kassem M. Human mesenchymal stem cells: From basic biology to clinical applications. Gene Therapy. 2008;15(2):109-16.
137. Boehler C, Asplund M. A detailed insight into drug delivery from PEDOT based on analytical methods: Effects and side effects. J Biomed Mater Res A 2015;103(3): 1200-7.
138. Ganeshan D, Chen S-C, Yin Z, Zheng Q. An anode buffer layer with size-controlled Ag nanoparticles for polymer solar cells with improved efficiencies. RSC Adv. 2015;5(21): 16153-61.
139. Chen P-Y, Li C-T, Lee C-P, Vittal R, Ho K-C. PEDOT-decorated nitrogen-doped graphene as the transparent composite film for the counter electrode of a dye-sensitized solar cell. Nano Energy. 2015;12(0):374-85.
140. Xiao S, Chen L, Tan L, Huang L, Wu F, Chen Y. Sulfonate Poly(aryl ether sulfone)-Modified PEDOT:PSS as hole transport layer and transparent electrode for high performance polymer solar cells. J Phys Chem C. 2015;119(4):1943-52.
141. Wang H, Kumar V. Transparent and conductive polysiloxanes/PEDOT: PSS nanocomposite thin films with a "water-impermeable" property to significantly enhance stability of organic-inorganic hybrid solar cells. RSC Adv. 2015;5(13):9650-7.
142. Shah MSAS, Muhammad S, Park JH, Yoon W-S, Yoo PJ. Incorporation of PEDOT: PSS into SnO2/reduced graphene oxide nanocomposite anodes for lithium-ion battery to achieve ultra-high capacity and cyclic stability. RSC Adv. 2015;5:13964-71.
143. Kim H, Lee Y-J, Park G-G, Park S-H, Choi Y-Y, Yoo Y. Fabrication of carbon paper containing PEDOT: PSS for use as a gas diffusion layer in proton exchange membrane fuel cells. Carbon. 2015;85:422-8.
144. Shahini A, Yazdimamaghani M, Walker KJ, Eastman MA, Hatami-Marbini H, Smith BJ, Ricci JL, Madihally SV, Vashaee D, Tayebi L. 3D conductive nanocomposite scaffold for bone tissue engineering. Int J Nanomed. 2014;9:167-81.
145. Tahmasbi Rad A, Ali N, Kotturi HSR, Yazdimamaghani M, Smay J, Vashaee D, Tayebi L. Conducting scaffolds for liver tissue engineering. J Biomed Mater Res A. 2014;102(11):4169-81.
146. Abidian MR, Daneshvar ED, Egeland BM, Kipke DR, Cederna PS, Urbanchek MG. Hybrid conducting polymer-hydrogel conduits for axonal growth and neural tissue engineering. Adv Healthc Mater. 2012;1(6): 762-7.
147. Kung TA, Langhals NB, Martin DC, Johnson PJ, Cederna PS, Urbanchek MG. Regenerative peripheral nerve interface viability and signal transduction with an implanted electrode. Plast Reconstr Surg. 2014;133(6): 1380-94.
148. Wrobel MR, Sundararaghavan HG. Directed migration in neural tissue engineering. Tissue Eng Part B Rev. 2013;20(2): 93-105.
149. Menorca RM, Fussell TS, Elfar JC. Nerve physiology: Mechanisms of injury and recovery. Hand Clin. 2013;29(3):317-30.
150. Ribeiro-Resende VT, Koenig B, Nichterwitz S, Oberhoffner S, Schlosshauer B. Strategies for inducing the formation of bands of Büngner in peripheral nerve regeneration. Biomater. 2009;30(29):5251-59.
151. Koppes AN, Nordberg AL, Paolillo GM, Goodsell NM, Darwish HA, Zhang L, Thompson DM. Electrical stimulation of Schwann cells promotes sustained increases in neurite outgrowth. Tissue Eng Part A. 2013;20(3-4): 494-506.
152. Jiang X, Lim SH, Mao H-Q, Chew SY. Current applications and future perspectives of artificial nerve conduits. Exp Neurol. 2010;223(1):86-101.
153. Dai L-G, Huang G-S, Hsu S-h. Sciatic nerve regeneration by cocultured Schwann cells and stem cells on microporous nerve conduits. Cell Transplant. 2013;22(11):2029-39.
154. Rodrigues MCO, Rodrigues AA, Glover LE, Voltarelli J, Borlongan CV. Peripheral nerve repair with cultured schwann cells: Getting closer to the clinics. Scientific World J. 2012;2012:1-10.
155. Baek S, Green RA, Poole-Warren LA. Effects of dopants on the biomechanical properties of conducting polymer films on platinum electrodes. J Biomed Mater Res A. 2014;102(8):2743-54.
156. Fonner JM, Forciniti L, Nguyen H, Byrne JD, Kou Y-F, Syeda-Nawaz J, Schmidt CE. Biocompatibility implications of polypyrrole synthesis techniques. Biomed Mater. 2008;3(3):034124.
157. Gaudet AD, Popovich PG, Ramer MS. Wallerian degeneration: Gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflammation. 2011;8(110): 1-13.
158. Hudson TW, Evans GR, Schmidt CE. Engineering strategies for peripheral nerve repair. Clin Plast Surg. 1999;26(4):617-28, ix.
159. Oh SH, Kim JH, Song KS, Jeon BH, Yoon JH, Seo TB, Namgung U, Lee IW, Lee JH. Peripheral nerve regeneration within an asymmetrically porous PLGA/Pluronic F127 nerve guide conduit. Biomaterials. 2008;29(11): 1601-9.
160. Bini T, Gao S, Xu X, Wang S, Ramakrishna S, Leong K. Peripheral nerve regeneration by microbraided poly (L-lactide-co-glycolide) biodegradable polymer fibers. J Biomed Mater Res A. 2004;68(2):286-95.
161. Evans G, Brandt K, Widmer M, Lu L, Meszlenyi R, Gupta P, Mikos A, Hodges J, Williams J, Gürlek A. In vivo evaluation of poly (L-lactic acid) porous conduits for peripheral nerve regeneration. Biomaterials. 1999;20(12): 1109-15.
162. Chang CJ. Effects of nerve growth factor from genipin-crosslinked gelatin in polycaprolactone conduit on peripheral nerve regeneration-in vitro and in vivo. J Biomed Mater Res A. 2009;91(2):586-96.
163. Yan Q, Yin Y, Li B. Use new PLGL-RGD-NGF nerve conduits for promoting peripheral nerve regeneration. Biomed Eng Online. 2012;11(36):1-16.
164. Chang C-J. The effect of pulse-released nerve growth factor from genipin-crosslinked gelatin in Schwann cell- seeded polycaprolactone conduits on large-gap peripheral nerve regeneration. Tissue Eng Part A. 2008;15(3):547-57.
165. Fu KY, Dai LG, Chiu IM, Chen JR, Hsu SH. Sciatic nerve regeneration by microporous nerve conduits seeded with glial cell line-derived neurotrophic factor or brain-derived neurotrophic factor gene transfected neural stem cells. Artif Organs. 2011;35(4):363-72.
166. Frattini F, Lopes FR, Almeida FM, Rodrigues RF, Boldrini LC, Tomaz MA, Baptista AF, Melo PA, Martinez AM. Mesenchymal stem cells in a polycaprolactone conduit promote sciatic nerve regeneration and sensory neuron survival after nerve injury. Tissue Eng Part A. 2012;18(19-20):2030-9.
167. Daly WT, Yao L, Abu-rub MT, O'Connell C, Zeugolis DI, Windebank AJ, Pandit AS. The effect of intraluminal contact mediated guidance signals on axonal mismatch during peripheral nerve repair. Biomaterials. 2012;33(28):6660-71.
168. Koh H, Yong T, Teo W, Chan C, Puhaindran M, Tan T, Lim A, Lim B, Ramakrishna S. In vivo study of novel nanofibrous intra-luminal guidance channels to promote nerve regeneration. J Neural Eng. 2010;7(4):046003.
169. Elzinga K, Tyreman N, Ladak A, Savaryn B, Olson J, Gordon T. Brief electrical stimulation improves nerve regeneration after delayed repair in Sprague Dawley rats. Exp Neurol. 2015;269:142-53.
170. Huang J, Lu L, Zhang J, Hu X, Zhang Y, Liang W, Wu S, Luo Z. Electrical stimulation to conductive scaffold promotes axonal regeneration and remyelination in a rat model of large nerve defect. PLoS One. 2012;7(6): E39526.
171. Cullen DK, Patel AR, Doorish JF, Smith DH, Pfister BJ. Developing a tissue-engineered neural-electrical relay using encapsulated neuronal constructs on conducting polymer fibers. J Neural Eng. 2008;5(4):374-84.