Time course of tissue remodelling and electrophysiology in the rat sciatic nerve after spiral cuff electrode implantation

Journal of Neuroimmunology

Volumn 185, Issue 1-2, 2007, Pages 103-114

  Thil, Marie Anne ^a   Duy, Dai Tran ^a   Colin, Ides M ^a   Delbeke, Jean ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Chronaxie; Electrode impedance; Nitric oxide synthase III; Rheobase; Vasa nervorum; Vascular endothelial growth factor

Indexed keywords

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRODE; ELECTROMYOGRAM; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; ENDONEURIUM; IMPEDANCE; IMPLANTATION; INFLAMMATORY CELL; NERVE FIBER DEGENERATION; NERVE FUNCTION; NERVE REGENERATION; NEUROPROTECTION; NONHUMAN; PERINEURIUM; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANIMALS; ELECTRIC IMPEDANCE; ELECTRODES, IMPLANTED; ELECTROMYOGRAPHY; MALE; RATS; RATS, WISTAR; SCIATIC NERVE; TIME FACTORS;

EID: 33947672394     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2007.01.021     Document Type: Article

References (51)

1. Agnew W.F., and McCreery D.B. Neural Prostheses (1990), Prentice Hall, New Jersey
2. Agnew W.F., McCreery D.B., Yuen T.G., and Bullara L.A. Histologic and physiologic evaluation of electrically stimulated peripheral nerve: considerations for the selection of parameters. Ann. Biomed. Eng. 17 (1989) 39-60
3. Creasey G.H., Ho C.H., Triolo R.J., Gater D.R., DiMarco A.F., Bogie K.M., and Keith M.W. Clinical applications of electrical stimulation after spinal cord injury. J. Spinal Cord Med. 27 (2004) 365-375
4. Donaldson N.D., Zhou L., Perkins T.A., Munih M., Haugland M., and Sinkjaer T. Implantable telemeter for long-term electroneurographic recordings in animals and humans. Med. Biol. Eng. Comput. 41 (2003) 654-664
5. Dvorak H.F. VPF/VEGF and the angiogenic response. Semin. Perinatol. 24 (2000) 75-78
6. Fagni L., and Bockaert J. Effects of nitric oxide on glutamate-gated channels and other ionic channels. J. Chem. Neuroanat. 10 (1996) 231-240
7. Grill W.M., and Mortimer J.T. Electrical properties of implant encapsulation tissue. Ann. Biomed. Eng. 22 (1994) 23-33
8. Grill W.M., and Mortimer J.T. Stability of the input-output properties of chronically implanted multiple contact nerve cuff stimulating electrodes. IEEE Trans. Rehabil. Eng. 6 (1998) 364-373
9. Grill W.M., and Mortimer J.T. Neural and connective tissue response to long-term implantation of multiple contact nerve cuff electrodes. J. Biomed. Mater. Res. 50 (2000) 215-226
10. Ignarro L.J. Biosynthesis and metabolism of endothelium-derived nitric-oxide. Annu. Rev. Pharmacol. Toxicol. 30 (1990) 535-560
11. Kalichman M.W., and Myers R.R. Transperineurial vessel constriction in an edematous neuropathy. J. Neuropathol. Exp. Neurol. 50 (1991) 408-418
12. Keilhoff G., Fansa H., and Wolf G. Nitric oxide synthase, an essential factor in peripheral nerve regeneration. Cell. Mol. Biol. (Noisy-le-grand) 49 (2003) 885-897
13. Kelliher E.M., and Rose T.L. Charge utilization in anodic rhodium oxide-films pulsed in carbonate-buffered saline. J. Electrochem. Soc. 136 (1989) 1765-1768
14. Kuo N.T., Benhayon D., Przybylski R.J., Martin R.J., and LaManna J.C. Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain. J. Appl. Physiol. 86 (1999) 260-264
15. Lambrechts D., Storkebaum E., and Carmeliet P. VEGF: necessary to prevent motoneuron degeneration, sufficient to treat ALS?. Trends Mol. Med. 10 (2004) 275-282
16. Lanmuller H., Ashley Z., Unger E., Sutherland H., Reichel M., Russold M., Jarvis J., Mayr W., and Salmons S. Implantable device for long-term electrical stimulation of denervated muscles in rabbits. Med. Biol. Eng. Comput. 43 (2005) 535-540
17. Larsen J.O., Thomsen M., Haugland M., and Sinkjaer T. Degeneration and regeneration in rabbit peripheral nerve with long-term nerve cuff electrode implant: a stereological study of myelinated and unmyelinated axons. Acta Neuropathol. (Berl.) 96 (1998) 365-378
18. Lee Y., and Shin T. Expression of constitutive endothelial and inducible nitric oxide synthase in the sciatic nerve of Lewis rats with experimental autoimmune neuritis. J. Neuroimmunol. 126 (2002) 78-85
19. Levy D., and Zochodne D.W. Local nitric oxide synthase activity in a model of neuropathic pain. Eur. J. Neurosci. 10 (1998) 1846-1855
20. Levy A.P., Levy N.S., Wegner S., and Goldberg M.A. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270 (1995) 13333-13340
21. Levy D., Tal M., Hoke A., and Zochodne D.W. Transient action of the endothelial constitutive nitric oxide synthase (ecNOS) mediates the development of thermal hypersensitivity following peripheral nerve injury. Eur. J. Neurosci. 12 (2000) 2323-2332
22. Loeb G.E., and Peck R.A. Cuff electrodes for chronic stimulation and recording of peripheral nerve activity. J. Neurosci. Methods 64 (1996) 95-103
23. Low P.A., Nukada H., Schmelzer J.D., Tuck R.R., and Dyck P.J. Endoneurial oxygen tension and radial topography in nerve edema. Brain Res. 341 (1985) 147-154
24. Lundborg G., Myers R., and Powell H. Nerve compression injury and increased endoneurial fluid pressure: a "miniature compartment syndrome". J. Neurol. Neurosurg. Psychiatry 46 (1983) 1119-1124
25. Mackinnon S.E., Dellon A.L., Hudson A.R., and Hunter D.A. Chronic nerve compression - an experimental model in the rat. Ann. Plast. Surg. 13 (1984) 112-120
26. McCreery D.B., Agnew W.F., Yuen T.G., and Bullara L.A. Damage in peripheral nerve from continuous electrical stimulation: comparison of two stimulus waveforms. Med. Biol. Eng. Comput. 30 (1992) 109-114
27. Michel O., Hess A., Krolzig M., Stennert E., Addick K., and Bloch W. Involvement of nitric oxide synthase in the physiology and pathophysiology of facial nerve function and dysfunction. Eur. Arch. Otorhinolaryngol. 257 (2000) 188-192
28. Moncada S., and Higgs E.A. Endogenous nitric oxide: physiology, pathology and clinical relevance. Eur. J. Clin. Investig. 21 (1991) 361-374
29. Murohara T., Asahara T., Silver M., Bauters C., Masuda H., Kalka C., Kearney M., Chen D., Symes J.F., Fishman M.C., Huang P.L., and Isner J.M. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J. Clin. Investig. 101 (1998) 2567-2578
30. Ochoa J., Folwer J.J., and Gilliatt R.W. Nature of the nerve lesion caused by a pneumatic tourniquet. Nature 233 (1971) 265
31. Prinz R.A., Nakamura-Pereira M., De-Ary-Pires B., Fernandes D.S., Fabiao-Gomes B.D., Bunn P.S., Martinez A.M., Pires-Neto M.A., and Ary-Pires R. Experimental chronic entrapment of the sciatic nerve in adult hamsters: an ultrastructural and morphometric study. Braz. J. Med. Biol. Res. 36 (2003) 1241-1245
32. Prodanov D., Thil M.A., Marani E., Delbeke J., and Holsheimer J. Three-dimensional topography of the motor endplates of the rat gastrocnemius muscle. Muscle Nerve 32 (2005) 292-302
33. Romero E., Denef J.F., Delbeke J., Robert A., and Veraart C. Neural morphological effects of long-term implantation of the self-sizing spiral cuff nerve electrode. Med. Biol. Eng. Comput. 39 (2001) 90-100
34. Rudic R.D., Shesely E.G., Maeda N., Smithies O., Segal S.S., and Sessa W.C. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Investig. 101 (1998) 731-736
35. Rydevik B., and Lundborg G. Permeability of intraneural microvessels and perineurium following acute, graded experimental nerve compression. Scand. J. Plast. Reconstr. Surg. 11 (1977) 179-187
36. Samii A., Unger J., and Lange W. Vascular endothelial growth factor expression in peripheral nerves and dorsal root ganglia in diabetic neuropathy in rats. Neurosci. Lett. 262 (1999) 159-162
37. Sasaki H., Kihara M., Zollman P.J., Nickander K.K., Smithson I.L., Schmelzer J.D., Willner C.L., Benarroch E.E., and Low P.A. Chronic constriction model of rat sciatic nerve: nerve blood flow, morphologic and biochemical alterations. Acta Neuropathol. (Berl.) 93 (1997) 62-70
38. Shrager P., Custer A.W., Kazarinova K., Rasband M.N., and Mattson D. Nerve conduction block by nitric oxide that is mediated by the axonal environment. J. Neurophysiol. 79 (1998) 529-536
39. Skold M.K., Marti H.H., Lindholm T., Linda H., Hammarberg H., Risling M., and Cullheim S. Induction of HIF1alpha but not HIF2alpha in motoneurons after ventral funiculus axotomy-implication in neuronal survival strategies. Exp. Neurol. 188 (2004) 20-32
40. Sondell M., Lundborg G., and Kanje M. Vascular endothelial growth factor stimulates Schwann cell invasion and neovascularization of acellular nerve grafts. Brain Res. 846 (1999) 219-228
41. Storkebaum E., Lambrechts D., and Carmeliet P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays 26 (2004) 943-954
42. Sunderland S. Nerves and Nerve Injuries (1972), Churchill Livingstone, Edinburg
43. Sweeney J.D., Ksienski D.A., and Mortimer J.T. A nerve cuff technique for selective excitation of peripheral-nerve trunk regions. IEEE Trans. Biomed. Eng. 37 (1990) 706-715
44. Thil M.A., Gerard B., Jarvis J.C., and Delbeke J. Two-way communication for programming and measurement in a miniature implantable stimulator. Med. Biol. Eng. Comput. 43 (2005) 528-534
45. Thil M.A., Vince V., Veraart C., Delbeke J., and Colin I.M. Nitric oxide synthases II and III and vascular endothelial growth factor are up-regulated in sciatic nerve after spiral cuff electrode implantation. J. Neuroimmunol. 166 (2005) 158-166
46. Thippeswamy T., and Morris R. Cyclic guanosine 3′,5′-monophosphate-mediated neuroprotection by nitric oxide in dissociated cultures of rat dorsal root ganglion neurones. Brain Res. 774 (1997) 116-122
47. Van Den Bosch L., Storkebaum E., Vleminckx V., Moons L., Vanopdenbosch L., Scheveneels W., Carmeliet P., and Robberecht W. Effects of vascular endothelial growth factor (VEGF) on motor neuron degeneration. Neurobiol. Dis. 17 (2004) 21-28
48. Veraart C., Grill W.M., and Mortimer J.T. Selective control of muscle activation with a multipolar nerve cuff electrode. IEEE Trans. Biomed. Eng. 40 (1993) 640-653
49. Vince V., Thil M.A., Gerard A.C., Veraart C., Delbeke J., and Colin I.M. Cuff electrode implantation around the sciatic nerve is associated with an upregulation of TNF-alpha and TGF-beta1. J. Neuroimmunol. 159 (2005) 75-86
50. Weibel E.R., Kistler G.S., and Scherle W.F. Practical stereological methods for morphometric cytology. J. Cell Biol. 30 (1966) 23-38
51. Zochodne D.W., Levy D., Zwiers H., Sun H., Rubin I., Cheng C., and Lauritzen M. Evidence for nitric oxide and nitric oxide synthase activity in proximal stumps of transected peripheral nerves. Neuroscience 91 (1999) 1515-1527