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Published in: Heart Failure Reviews 2/2011

01-03-2011

Histopathology of the stimulated Vagus nerve: primum non nocere

Authors: Mark L. Cohen, Zhanna Georgievskaya

Published in: Heart Failure Reviews | Issue 2/2011

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Abstract

A primary concern in the utilization of implantable neural interfaces for the treatment of medical diseases is to follow the Hippocratic dictum: First, do no harm. If we are to avoid harm to the Vagus nerve in our use of stimulatory electrodes in the treatment of heart failure, we must understand the structural and functional elements that comprise peripheral nerves, their susceptibility to various types of injury that might be expected to occur secondary to functional electrical stimulation and how to separate the various components of the response of peripheral nervous system elements to stresses that may occur in the complex interactions that take place between electrode and nerve. To this end, we review the functional histology of peripheral nerve, followed by a consideration of salient types of nerve injuries, which have been elucidated through the combination of careful observations of human disease and well-constructed experimental models. We then examine the extant literature on stimulation-induced nerve injury in light of recent developments in the understanding of electropermeabilization of biological membranes. Finally, we briefly discuss our experience using the CardioFit™ electrode on the canine Vagus nerve.
Literature
1.
go back to reference Volta A (1800) On the electricity excited by the mere contact of conducting substances of different kinds. Philos Trans 90:403–431CrossRef Volta A (1800) On the electricity excited by the mere contact of conducting substances of different kinds. Philos Trans 90:403–431CrossRef
2.
go back to reference Jallabert J (1748) Experiences sur l’electricite, avec quelque conjectures sur la cause de ses effects. Geneve, Barrillot & Fils, Paris Jallabert J (1748) Experiences sur l’electricite, avec quelque conjectures sur la cause de ses effects. Geneve, Barrillot & Fils, Paris
3.
go back to reference Shepard GM (2010) Creating modern neuroscience: the revolutionary 1950s. Oxford University Press, New York Shepard GM (2010) Creating modern neuroscience: the revolutionary 1950s. Oxford University Press, New York
4.
go back to reference Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544PubMed Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500–544PubMed
5.
go back to reference Elmqvist R, Senning A (1960) An implantable pacemaker for the heart. In Smyth CN (ed) Proceedings of the Second International Conference on Medical Electronics: Paris, France June 24–27, 1959. Tliffe & Sons, London, pp. 253–254 Elmqvist R, Senning A (1960) An implantable pacemaker for the heart. In Smyth CN (ed) Proceedings of the Second International Conference on Medical Electronics: Paris, France June 24–27, 1959. Tliffe & Sons, London, pp. 253–254
6.
go back to reference Zanchetti A, Wang SC, Moruzzi G (1952) The effect of vagal afferent stimulation on the EEG pattern of the cat. Electroencephalogr Clin Neurophysiol 4:357–361CrossRefPubMed Zanchetti A, Wang SC, Moruzzi G (1952) The effect of vagal afferent stimulation on the EEG pattern of the cat. Electroencephalogr Clin Neurophysiol 4:357–361CrossRefPubMed
7.
go back to reference Penry JK, Dean JC (1990) Prevention of intractable partial seizures by intermittent vagal stimulation in humans: preliminary results. Epilepsia 31(Suppl 2):S40CrossRefPubMed Penry JK, Dean JC (1990) Prevention of intractable partial seizures by intermittent vagal stimulation in humans: preliminary results. Epilepsia 31(Suppl 2):S40CrossRefPubMed
8.
go back to reference Olshansky B, Sabbah HN, Hauptman PJ, Colucci WS (2008) Parasympathetic nervous system and heart failure: pathophysiology and potential implications for therapy. Circulation 118:863–871CrossRefPubMed Olshansky B, Sabbah HN, Hauptman PJ, Colucci WS (2008) Parasympathetic nervous system and heart failure: pathophysiology and potential implications for therapy. Circulation 118:863–871CrossRefPubMed
9.
go back to reference Air EL, Ghomri YM, Tyagi R, Grande AW, Crone K, Mangano FT (2009) Management of vagal nerve stimulator infections: do they need to be removed? J Neurosurg Pediatr 3:73–78CrossRefPubMed Air EL, Ghomri YM, Tyagi R, Grande AW, Crone K, Mangano FT (2009) Management of vagal nerve stimulator infections: do they need to be removed? J Neurosurg Pediatr 3:73–78CrossRefPubMed
10.
go back to reference Spitz MC, Winston KR, Maa EH, Ojemann SG (2010) Insulation discontinuity in a Vagus nerve stimulator lead: a treatable cause of intolerable stimulation-related symptoms. J Neurosurg 112:829–831CrossRefPubMed Spitz MC, Winston KR, Maa EH, Ojemann SG (2010) Insulation discontinuity in a Vagus nerve stimulator lead: a treatable cause of intolerable stimulation-related symptoms. J Neurosurg 112:829–831CrossRefPubMed
11.
go back to reference Hartline DK, Colman DR (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17:R29–R35CrossRefPubMed Hartline DK, Colman DR (2007) Rapid conduction and the evolution of giant axons and myelinated fibers. Curr Biol 17:R29–R35CrossRefPubMed
12.
go back to reference Dyck PJ, Lais AC, Giannini C, Engelstad JK (1990) Structural alterations of nerve during cuff compression. Proc Natl Acad Sci USA 87:9828–9832CrossRefPubMed Dyck PJ, Lais AC, Giannini C, Engelstad JK (1990) Structural alterations of nerve during cuff compression. Proc Natl Acad Sci USA 87:9828–9832CrossRefPubMed
13.
go back to reference Wang Y, Kawamura N, Schmelzer JD, Schmeichel AM, Low PA (2008) Decreased peripheral nerve damage after ischemia-reperfusion injury in mice lacking TNF-alpha. J Neurol Sci 267:107–111CrossRefPubMed Wang Y, Kawamura N, Schmelzer JD, Schmeichel AM, Low PA (2008) Decreased peripheral nerve damage after ischemia-reperfusion injury in mice lacking TNF-alpha. J Neurol Sci 267:107–111CrossRefPubMed
14.
go back to reference Iida H, Nagasaka T, Shindo K, Shiozawa Z (2009) Effect of the free radical scavenger edaravone on peripheral nerve ischemia-reperfusion injury. Muscle Nerve 40:582–588CrossRefPubMed Iida H, Nagasaka T, Shindo K, Shiozawa Z (2009) Effect of the free radical scavenger edaravone on peripheral nerve ischemia-reperfusion injury. Muscle Nerve 40:582–588CrossRefPubMed
15.
go back to reference Pham K, Gupta R (2009) Understanding the mechanisms of entrapment neuropathies. Neurosurg Focus 26:E7CrossRefPubMed Pham K, Gupta R (2009) Understanding the mechanisms of entrapment neuropathies. Neurosurg Focus 26:E7CrossRefPubMed
16.
go back to reference Krarup C, Moldovan M (2009) Nerve conduction and excitability studies in peripheral nerve disorders. Curr Opin Neurol 22:460–466CrossRefPubMed Krarup C, Moldovan M (2009) Nerve conduction and excitability studies in peripheral nerve disorders. Curr Opin Neurol 22:460–466CrossRefPubMed
17.
go back to reference Mozaffar T, Strandberg E, Abe K, Hilgenberg LG, Smith MA, Gupta R (2009) Neuromuscular junction integrity after chronic nerve compression injury. J Orthop Res 27:114–119CrossRefPubMed Mozaffar T, Strandberg E, Abe K, Hilgenberg LG, Smith MA, Gupta R (2009) Neuromuscular junction integrity after chronic nerve compression injury. J Orthop Res 27:114–119CrossRefPubMed
18.
go back to reference Gupta R, Rowshan K, Chao T, Mozaffar T, Steward O (2004) Chronic nerve compression induces local demyelination and remyelination in a rat model of carpal tunnel syndrome. Exp Neurol 187:500–508CrossRefPubMed Gupta R, Rowshan K, Chao T, Mozaffar T, Steward O (2004) Chronic nerve compression induces local demyelination and remyelination in a rat model of carpal tunnel syndrome. Exp Neurol 187:500–508CrossRefPubMed
19.
go back to reference Gupta R, Steward O (2003) Chronic nerve compression induces concurrent apoptosis and proliferation of Schwann cells. J Comp Neurol 461:174–186CrossRefPubMed Gupta R, Steward O (2003) Chronic nerve compression induces concurrent apoptosis and proliferation of Schwann cells. J Comp Neurol 461:174–186CrossRefPubMed
20.
go back to reference Pham K, Nassiri N, Gupta R (2009) c-Jun, krox-20, and integrin beta4 expression following chronic nerve compression injury. Neurosci Lett 465:194–198CrossRefPubMed Pham K, Nassiri N, Gupta R (2009) c-Jun, krox-20, and integrin beta4 expression following chronic nerve compression injury. Neurosci Lett 465:194–198CrossRefPubMed
21.
go back to reference Anderson JM, Rodriguez A, Chang DT (2008) Foreign body reaction to biomaterials. Semin Immunol 20:86–100CrossRefPubMed Anderson JM, Rodriguez A, Chang DT (2008) Foreign body reaction to biomaterials. Semin Immunol 20:86–100CrossRefPubMed
22.
go back to reference Ratner BD, Bryant SJ (2004) Biomaterials: where we have been, where we are going. Annu Rev Biomed Eng 6:41–75CrossRefPubMed Ratner BD, Bryant SJ (2004) Biomaterials: where we have been, where we are going. Annu Rev Biomed Eng 6:41–75CrossRefPubMed
23.
go back to reference Grill WM, Norman SE, Bellamkonda RV (2009) Implanted neural interfaces: biochallenges and engineered solutions. Annu Rev Biomed Eng 11:1–24CrossRefPubMed Grill WM, Norman SE, Bellamkonda RV (2009) Implanted neural interfaces: biochallenges and engineered solutions. Annu Rev Biomed Eng 11:1–24CrossRefPubMed
24.
go back to reference Albayrak BS, Ismailoglu O, Ilbay K, Yaka U, Tanriover G, Gorgulu A, Demir N (2010) Doxorubicin for prevention of epineurial fibrosis in a rat sciatic nerve model: outcome based on gross postsurgical, histopathological, and ultrastructural findings. J Neurosurg: spine 12:327–333CrossRef Albayrak BS, Ismailoglu O, Ilbay K, Yaka U, Tanriover G, Gorgulu A, Demir N (2010) Doxorubicin for prevention of epineurial fibrosis in a rat sciatic nerve model: outcome based on gross postsurgical, histopathological, and ultrastructural findings. J Neurosurg: spine 12:327–333CrossRef
25.
go back to reference Agnew WF, McCreery DB, Yuen TG, Bullara LA (1989) Histologic and physiologic evaluation of electrically stimulated peripheral nerve: considerations for the selection of parameters. Ann Biomed Eng 17:39–60CrossRefPubMed Agnew WF, McCreery DB, Yuen TG, Bullara LA (1989) Histologic and physiologic evaluation of electrically stimulated peripheral nerve: considerations for the selection of parameters. Ann Biomed Eng 17:39–60CrossRefPubMed
26.
go back to reference Agnew WF, McCreery DB (1990) Considerations for safety with chronically implanted nerve electrodes. Epilepsia 31:S27–S32CrossRefPubMed Agnew WF, McCreery DB (1990) Considerations for safety with chronically implanted nerve electrodes. Epilepsia 31:S27–S32CrossRefPubMed
27.
go back to reference Escoffre JM, Portet T, Wasungu L, Teissié J, Dean D, Rols MP (2009) What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 41:286–295CrossRefPubMed Escoffre JM, Portet T, Wasungu L, Teissié J, Dean D, Rols MP (2009) What is (still not) known of the mechanism by which electroporation mediates gene transfer and expression in cells and tissues. Mol Biotechnol 41:286–295CrossRefPubMed
28.
go back to reference Chen W, Lee RC (1994) Altered ion channel conductance and ionic selectivity induced by large imposed membrane potential pulse. Biophys J 67:603–612CrossRefPubMed Chen W, Lee RC (1994) Altered ion channel conductance and ionic selectivity induced by large imposed membrane potential pulse. Biophys J 67:603–612CrossRefPubMed
29.
go back to reference Merrill DR, Bikson M, Jefferys JG (2005) Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Meth 141:171–198CrossRef Merrill DR, Bikson M, Jefferys JG (2005) Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosci Meth 141:171–198CrossRef
30.
go back to reference Vernier PT, Levine ZA, Wu YH, Joubert V, Ziegler MJ, Mir LM, Tieleman DP (2009) Electroporating fields target oxidatively damaged areas in the cell membrane. PLoS One 4:e7966CrossRefPubMed Vernier PT, Levine ZA, Wu YH, Joubert V, Ziegler MJ, Mir LM, Tieleman DP (2009) Electroporating fields target oxidatively damaged areas in the cell membrane. PLoS One 4:e7966CrossRefPubMed
31.
go back to reference Aspalter M, Vyas A, Feiner J, Griffin J, Brushart T, Redett R (2009) Modification of Schwann cell gene expression by electroporation in vivo. J Neurosci Meth 176:96–103CrossRef Aspalter M, Vyas A, Feiner J, Griffin J, Brushart T, Redett R (2009) Modification of Schwann cell gene expression by electroporation in vivo. J Neurosci Meth 176:96–103CrossRef
32.
go back to reference Hoffman HH, Schnitzlein HN (1961) The numbers of nerve fibers in the Vagus nerve of man. Anat Rec 139:429–435CrossRefPubMed Hoffman HH, Schnitzlein HN (1961) The numbers of nerve fibers in the Vagus nerve of man. Anat Rec 139:429–435CrossRefPubMed
33.
go back to reference Schnitzlein HN, Rowe LC, Hoffman HH (1958) The myelinated component of the Vagus nerves in man. Anat Rec 131:649–667CrossRef Schnitzlein HN, Rowe LC, Hoffman HH (1958) The myelinated component of the Vagus nerves in man. Anat Rec 131:649–667CrossRef
34.
go back to reference Feirabend HK, Choufoer H, Ploeger S (1998) Preservation and staining of myelinated nerve fibers. Methods 15:123–131CrossRefPubMed Feirabend HK, Choufoer H, Ploeger S (1998) Preservation and staining of myelinated nerve fibers. Methods 15:123–131CrossRefPubMed
Metadata
Title
Histopathology of the stimulated Vagus nerve: primum non nocere
Authors
Mark L. Cohen
Zhanna Georgievskaya
Publication date
01-03-2011
Publisher
Springer US
Published in
Heart Failure Reviews / Issue 2/2011
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI
https://doi.org/10.1007/s10741-010-9182-6

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