Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Journal of NeuroEngineering and Rehabilitation
Published in: Journal of NeuroEngineering and Rehabilitation 1/2014

Open Access 01-12-2014 | Research

Biomechanical and functional variation in rat sciatic nerve following cuff electrode implantation

Authors: Stephen M Restaino, Erkinay Abliz, Kelliann Wachrathit, Victor Krauthamer, Sameer B Shah

Published in: Journal of NeuroEngineering and Rehabilitation | Issue 1/2014

Login to get access

Abstract

Background

Nerve cuff electrodes are commonly and successfully used for stimulating peripheral nerves. On the other hand, they occasionally induce functional and morphological changes following chronic implantation, for reasons not always clear. We hypothesize that restriction of nerve mobility due to cuff implantation may alter nerve conduction.

Methods

We quantified acute changes in nerve-muscle electrophysiology, using electromyography, and nerve kinematics in anesthetized Sprague Dawley rat sciatic nerves during controlled hindlimb joint movement. We compared electrophysiological and biomechanical response in uncuffed nerves and those secured within a cuff electrode using analysis of variance (ANOVA) and regression analysis.

Results

Tethering resulting from cuff implantation resulted in altered nerve strain and a complex biomechanical environment during joint movement. Coincident with biomechanical changes, electromyography revealed significantly increased variability in the response of conduction latency and amplitude in cuffed, but not free, nerves following joint movement.

Conclusion

Our findings emphasize the importance of the mechanical interface between peripheral nerves and their devices on neurophysiological performance. This work has implications for nerve device design, implantation, and prediction of long-term efficacy.
Literature
1.
Rodriguez FJ, Ceballos D, Schüttler M, Valero A, Valderrama E, Stieglitz T, Navarro X: Polyimide cuff electrodes for peripheral nerve stimulation. J Neurosci Methods 2000, 98: 105-118.CrossRefPubMed
2.
Loeb GE, Peck RA: Cuff electrodes for chronic stimulation and recording of peripheral nerve activity. J Neurosci Methods 1996, 64: 95-103.CrossRefPubMed
3.
Garde K, Keefer E, Botterman B, Galvan P, Romero MI: Early Interfaced Neural Activity from Chronic Amputated Nerves. Front Neuroengineering 2009, 2: 5.CrossRefPubMedCentral
4.
Fugleholm K, Schmalbruch H, Krarup C: Early peripheral nerve regeneration after crushing, sectioning, and freeze studied by implanted electrodes in the cat. J Neurosci 1994, 14: 2659-2673.PubMed
5.
Lawrence SM, Dhillon GS, Horch KW: Fabrication and characteristics of an implantable, polymer-based, intrafascicular electrode. J Neurosci Methods 2003, 131: 9-26.CrossRefPubMed
6.
Lawrence SM, Dhillon GS, Jensen W, Yoshida K, Horch KW: Acute peripheral nerve recording Characteristics of polymer-based longitudinal intrafascicular electrodes. IEEE Trans Neural Syst Rehabil Eng 2004, 12: 345-348.CrossRefPubMed
7.
Micera S, Navarro X, Carpaneto J, Citi L, Tonet O, Rossini PM, Carrozza MC, Hoffmann KP, Vivo M, Yoshida K, Dario P: On the Use of Longitudinal Intrafascicular Peripheral Interfaces for the Control of Cybernetic Hand Prostheses in Amputees. IEEE Trans Neural Syst Rehabil Eng 2008, 16: 453-472.CrossRefPubMed
8.
Navarro X, Lago N, Vivo M, Yoshida K, Koch KP, Poppendieck W, Micera S: Neurobiological evaluation of thin-film longitudinal intrafascicular electrodes as a peripheral nerve interface. Rehabi Robot, ICORR 2007 IEEE 10th Int Conf 2007, 2007: 643-649.CrossRef
9.
Badia J, Boretius T, Pascual-Font A, Udina E, Stieglitz T, Navarro X: Biocompatibility of Chronically Implanted Transverse Intrafascicular Multichannel Electrode (TIME) in the Rat Sciatic Nerve. IEEE Trans Biomed Eng 2011, 58: 2324-2332.CrossRef
10.
Boretius T, Badia J, Pascual-Font A, Schuettler M, Navarro X, Yoshida K, Stieglitz T: A transverse intrafascicular multichannel electrode (TIME) to interface with the peripheral nerve. Biosens Bioelectron 2010, 26: 62-69.CrossRefPubMed
11.
Branner A, Normann RA: A multielectrode array for intrafascicular recording and stimulation in sciatic nerve of cats. Brain Research Bulliten 2000, 51: 293-306.CrossRef
12.
Branner A, Stein RB, Normann RA: Selective stimulation and recording using a slanted multielectrode array. Eng Med Biol 1999 21st Annual Conf the 1999 Annual Fall Meeting of the Biomed Eng Soc] BMES/EMBS Conf 1999, 371: 377.
13.
Branner A, Stein RB, Normann RA: Selective Stimulation of Cat Sciatic Nerve Using an Array of Varying-Length Microelectrodes. J Neurophysiol 2001, 85: 1585-1594.PubMed
14.
Clark GA, Ledbetter NM, Warren DJ, Harrison RR: Recording sensory and motor information from peripheral nerves with Utah Slanted Electrode Arrays. Eng Med Biol Soc EMBC, 2011 Annual Int Conf the IEEE 2011, 2011: 4641-4644.CrossRef
15.
Delbeke J, Oozeer M, Veraart C: Position, size and luminosity of phosphenes generated by direct optic nerve stimulation. Vision Res 2003, 43: 1091-1102.CrossRefPubMed
16.
Delbeke J, Wanet-Defalque MC, Gérard B, Troosters M, Michaux G, Veraart C: The microsystems based visual prosthesis for optic nerve stimulation. Artif Organs 2012, 26: 232-234.CrossRef
17.
Veraart C, Raftopoulos C, Mortimer JT, Delbeke J, Pins D, Michaux G, Vanlierde A, Parrini S, Wanet-Defalque M-C: Visual sensations produced by optic nerve stimulation using an implanted self-sizing spiral cuff electrode. Brain Res 1998, 813: 181-186.CrossRefPubMed
18.
Veraart C, Wanet-Defalque MC, Gérard B, Vanlierde A, Delbeke J: Pattern Recognition with the Optic Nerve Visual Prosthesis. Artif Organs 2012, 27: 996-1004.CrossRef
19.
DeGiorgio CM, Schachter SC, Handforth A, Salinsky M, Thompson J, Uthman B, Reed R, Collins S, Tecoma E, Morris GL, Vaughn B, Naritoku DK, Henry T, Labar D, Gilmartin R, Labiner D, Osorio I, Ristanovic R, Jones J, Murphy J, Ney G, Wheless J, Lewis P, Heck C: Prospective Long‒Term Study of Vagus Nerve Stimulation for the Treatment of Refractory Seizures. Epilepsia 2012, 41: 1195-1200.CrossRef
20.
Krahl SE, Clark KB, Smith DC, Browning RA: Locus Coeruleus Lesions Suppress the Seizure‒Attenuating Effects of Vagus Nerve Stimulation. Epilepsia 2012, 39: 709-714.CrossRef
21.
Krahl SE, Senanayake SS, Pekary AE, Sattin A: Vagus nerve stimulation (VNS) is effective in a rat model of antidepressant action. J Psychiatr Res 2004, 38: 237-240.CrossRefPubMed
22.
Naritoku DK, Terry WJ, Helfert RH: Regional induction of fos immunoreactivity in the brain by anticonvulsant stimulation of the vagus nerve. Epilepsy Res 1995, 22: 53-62.CrossRefPubMed
23.
Takaya M, Terry WJ, Naritoku DK: Vagus Nerve Stimulation Induces a Sustained Anticonvulsant Effect. Epilepsia 2012, 37: 111-1116.
24.
Lundgren J, Amark P, Blennow G, Stromblad LG, Wallstedt L: Vagus nerve stimulation in 16 children with refractory epilepsy. Epilepsia 1998, 39: 809-813.CrossRefPubMed
25.
Lundy DS, Casiano RR, Landy HJ, Gallo J, Gallo B, Ramsey RE: Effects of vagal nerve stimulation on laryngeal function. J Voice 1993, 7: 359-364.CrossRefPubMed
26.
Sahin M, Durand DM: Improved nerve cuff electrode recordings with subthreshold anodic currents. IEEE Trans Biomed Eng 1998, 45: 1044-1050.CrossRefPubMed
27.
Sahin M, Haxhiu MA, Durand DM, Dreshaj IA, Sahin M, Haxhiu MA, Durand DM, Dreshaj IA: Spiral nerve cuff electrode for recordings of respiratory output. J Appl Physiol 1997, 83: 317-322.PubMed
28.
DiMarco AF, Onders RP, Kowalski KE, Miller ME, Ferek S, Mortimer JT: Phrenic Nerve Pacing in a Tetraplegic Patient via Intramuscular Diaphragm Electrodes. Am J Respir Crit Care Med 2002, 166: 1604-1606.CrossRefPubMed
29.
Weese-Mayer DE, Silvestri JM, Kenny AS, Ilbawi MN, Hauptman SA, Lipton JW, Talonen PP, Garcia HG, Watt JW, Exner G, Baer GA, Elefteriades JA, Peruzzi WT, Alex CG, Harlid R, Vincken W, Davis GM, Decramer M, Kuenzle C, Saeterhaug A, Schöber JG: Diaphragm Pacing with a Quadripolar Phrenic Nerve Electrode: An International Study. Pacing Clin Electrophysiology 2012, 19: 1311-1319.CrossRef
30.
Gustafson KJ, Pinault GCJ, Neville JJ, Syed I, Davis JA, Jean-Claude J, Triolo RJ: Fascicular anatomy of human femoral nerve: Implications for neural prostheses using nerve cuff electrodes. J Rehabil Res Dev 2009, 46: 973-984.CrossRefPubMedPubMedCentral
31.
Navarro X, Krueger TB, Lago N, Micera S, Stieglitz T, Dario P: A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems. J Peripher Nerv Syst 2012, 10: 229-258.CrossRef
32.
Frankel MA, Dowden BR, Mathews VJ, Normann RA, Clark GA, Meek SG: Multiple-Input Single-Output Closed-Loop Isometric Force Control Using Asynchronous Intrafascicular Multi-Electrode Stimulation. IEEE Trans Neural Syst Rehabil Eng 2011, 19: 325-332.CrossRefPubMed
33.
Caparso AV, Durand DM, Mansour JM, Caparso AV, Durand DM, Mansour JM: A Nerve Cuff Electrode for Controlled Reshaping of Nerve Geometry. J Biomater Appl 2009, 24: 247-273.CrossRefPubMedPubMedCentral
34.
Polasek KH, Hoyen HA, Keith MW, Tyler DJ: Human Nerve Stimulation Thresholds and Selectivity Using a Multi-contact Nerve Cuff Electrode. IEEE Trans Neural Syst Rehabil 2007, 15: 76-82. EngCrossRef
35.
Edell DJ, Churchill JN, Gourley IM: Biocompatibility of a Silicon Based Peripheral Nerve Electrode. Biomater Med Devices Artif Organs 1982, 10: 103-122.CrossRefPubMed
36.
Murphy B, Krieger C, Hoffer J-A: Chronically implanted epineural electrodes for repeated assessment of nerve conduction velocity and compound action potential amplitude in rodents. J Neurosci Methods 2004, 132: 25-33.CrossRefPubMed
37.
Larsen JO, Thomsen M, Haugland M, 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 1998, 96: 365-378.CrossRefPubMed
38.
Grill WM, Mortimer JT: Electrical Properties of Implant Encapsulation Tissue. Ann Biomed Eng 1994, 22: 23-33.CrossRefPubMed
39.
Leventhal DK, Cohen M, Durand DM: Chronic histological effects of the flat interface nerve electrode. J Neural Eng 2006, 3: 102.CrossRefPubMed
40.
Vince V, Brelen ME, Delbeke J, Colin IM: Anti-TNF-α reduces the inflammatory reaction associated with cuff electrode implantation around the sciatic nerve. J Neuroimmunol 2005, 165: 121-128.CrossRefPubMed
41.
Vince V, Thil M-A, Gérard A-C, Veraart C, Delbeke J, Colin IM: Cuff electrode implantation around the sciaticnerve is associated with an upregulation of TNF-α and TGF-β1. J Neuroimmunol 2005, 159: 75-86.CrossRefPubMed
42.
Thil M-A, Duy DT, Colin IM, Delbeke J: Timecourse of tissue remodelling and electrophysiology in the rat sciatic nerve after spiral cuff electrode implantation. J Neuroimmunol 2007, 185: 103-114.CrossRefPubMed
43.
Grill WM, Mortimer JT: Neural and connective tissue response to long-term implantation of multiple contact nerve cuff electrodes. J Biomed Mater Res 2000, 50: 215-226.CrossRefPubMed
44.
Gupta R, Nassiri N, Hazel A, Bathen M, Mozaffar T: Chronic nerve compression alters Schwann cell myelin architecture in a murine model. Muscle Nerve 2012, 45: 231-241.CrossRefPubMedPubMedCentral
45.
Gupta R, Rowshan K, Chao T, Mozaffar T, Steward O: Chronic nerve compression induces local demyelination and remyelination in a rat model of carpal tunnel syndrome. Exp Neurol 2004, 187: 500-508.CrossRefPubMed
46.
Zumsteg D, Jenny D, Wieser HG: Vocal cord adduction during vagus nerve stimulation for treatment of epilepsy. Neurology 2000, 54: 1388-1389.CrossRefPubMed
47.
Boyd BS, Puttlitz C, Gan J, Topp KS: Strain and excursion in the rat sciatic nerve during a modified straight leg raise are altered after traumatic nerve injury. J Orthop Res 2012, 23: 764-770.CrossRef
48.
Topp KS, Boyd BS: Structure and Biomechanics of Peripheral Nerves: Nerve Responses to Physical Stresses and Implications for Physical Therapist Practice. Phys Ther 2006, 86: 92-109.PubMed
49.
Wright TW, Glowczewskie F Jr, Cowin D, Wheeler DL: Ulnar nerve excursion and strain at the elbow and wrist associated with upper extremity motion. J Hand Surg [Am] 2001, 26: 655-662.CrossRef
50.
Wright TW, Glowczewskie F, Wheeler D, Miller G, Cowin D: Excursion and strain of the median nerve. J Bone Joint Surg Am 1996, 78: 1897-1903.PubMed
51.
Wall EJ, Kwan MK, Rydevik BL, Woo SL, Garfin SR: Stress relaxation of a peripheral nerve. J Hand Surg [Am] 1991, 16: 859-863.CrossRef
52.
Kwan MK, Wall EJ, Massie J, Garfin SR: Strain, stress and stretch of peripheral nerve. Rabbit experiments in vitro and in vivo. Acta Orthop Scand 1992, 63: 267-272.CrossRefPubMed
53.
Phillips JB, Smit X, De Zoysa N, Afoke A, Brown RA: Peripheral nerves in the rat exhibit localized heterogeneity of tensile properties during limb movement. J Physiol 2004, 557: 879-887.CrossRefPubMedPubMedCentral
54.
Wall E, Massie J, Kwan M, Rydevik B, Myers R, Garfin S, Wall E, Massie J, Kwan M, Rydevik B, Myers R, Garfin S: Experimental stretch neuropathy. Changes in nerve conduction under tension. J Bone Joint Surg (Br) 1992, 74: 126-129.
55.
Highet WB, Sanders FK: The effects of stretching nerves after suture. Br J Surg 2012, 30: 355-369.CrossRef
56.
Naples GG, Mortimer JT, Scheiner A, Sweeney JD: A spiral nerve cuff electrode for peripheral nerve stimulation. IEEE Trans on Biomed Eng 1988, 35: 905-916.CrossRef
57.
Rydevik BL, Kwan MK, Myers RR, Brown RA, Triggs KJ, Woo SL, Garfin SR: An in vitro mechanical and histological study of acute stretching on rabbit tibial nerve. J Orthop Res 1990, 8: 694-701.CrossRefPubMed
58.
Rempel DM, Diao E: Entrapment neuropathies: pathophysiology and pathogenesis. J Electromyogr Kinesiol 2004, 14: 71-75.CrossRefPubMed
59.
Nishiura Y, Hara Y, Yoshii Y, Ochiai N: Gradual stretching of the proximal nerve stump induces the growth of regenerating sprouts in rats. J Orthop Res 2008, 26: 1012-1017.CrossRefPubMed
60.
Nishiura Y, Yamada Y, Hara Y, Ichimura H, Yoshii Y, Ochiai N: Repair of peripheral nerve defect with direct gradual lengthening of the proximal nerve stump in rats. J Orthop Res 2006, 24: 2246-2253.CrossRefPubMed
61.
Loverde JR, Ozoka VC, Aquino R, Lin L, Pfister BJ: Live imaging of axon stretch growth in embryonic and adult neurons. J Neurotrauma 2011, 28: 2389-2403.CrossRefPubMed
62.
Kupa EJ, Roy SH, Kandarian SC, Luca CJD: Effects of muscle fiber type and size on EMG median frequency and conduction velocity. J Appl Physiol 1995, 79: 23-32.PubMed
63.
Stecker MM, Baylor K, Chan YM: Acute nerve compression and the compound muscle action potential. J Brachial Plex and Peripher Nerve Inj 2008, 3: 1.
64.
Parry GJ, Cornblath DR, Brown MJ: Transient conduction block following acute peripheral nerve ischemia. Muscle Nerve 1985, 8: 409-412.CrossRefPubMed
65.
Kiechl S: 2013. Clinical and Electrodiagnostic Work-up of Peripheral Nerve Lesions. In Medical Radiology, Diagnostic Imaging: High-Resolution Sonography of the Peripheral Nervous System Berlin. Heidelberg: Springer-Verlag Berlin Heidelberg; 2008:43-70.CrossRef
66.
Schiefer MA, Polasek KH, Triolo RJ, Pinault GCJ, Tyler DJ: Selective stimulation of the human femoral nerve with a flat interface nerve electrode. J Neural Eng 2010, 7: 26006.CrossRefPubMedPubMedCentral
67.
Pearl PL, Conry JA, Yaun A, Taylor JL, Heffron AM, Sigman M, Tsuchida TN, Elling NJ, Bruce DA, Gaillard WD: Misidentification of vagus nerve stimulator for intravenous access and other major adverse events. Pediatr Neurol 2008, 38: 248-251.CrossRefPubMed
68.
Ng WH, Donner E, Go C, Abou-Hamden A, Rutka JT: Revision of vagal nerve stimulation (VNS) electrodes: review and report on use of ultra-sharp monopolar tip. Childs Nerv Syst 2010, 26: 1081-1084.CrossRefPubMed
69.
O’Neill BR, Wilberger JE: Revision of vagal nerve stimulator electrodes through a posterior cervical triangle approach: technical note. Neurosurgery 2010, 67: 457-460.PubMed
70.
Ortler M, Unterhofer C, Dobesberger J, Haberlandt E, Trinka E: Complete removal of vagus nerve stimulator generator and electrodes. J Neurosurg Pediatr 2010, 5: 191-194.CrossRefPubMed
71.
Santos PM: Evaluation of laryngeal function after implantation of the vagus nerve stimulation device. Otolaryngol Head Neck Surg 2003, 129: 269-273.CrossRefPubMed
72.
Kim DH, Lu N, Ma R, Kim YS, Kim RH, Wang S, Wu J, Won SM, Tao H, Islam A, Yu KJ, Kim TI, Chowdhury R, Ying M, Xu L, Li M, Chung HJ, Keum H, McCormick M, Liu P, Zhang YW, Omenetto FG, Huang Y, Coleman T, Rogers JA: Epidermal Electronics. Science 2011, 333: 838-843.CrossRefPubMed
73.
Farole A, Jamal BT: A Bioabsorbable Collagen Nerve Cuff (NeuraGen) for Repair of Lingual and Inferior Alveolar Nerve Injuries: A Case Series. J Oral Maxillofac Surg 2008, 66: 2058-2062.CrossRefPubMed
74.
Archibald SJ, Krarup C, Shefner J, Li ST, Madison RD: A collagen‒based nerve guide conduit for peripheral nerve repair: An electrophysiological study of nerve regeneration in rodents and nonhuman primates. J Comp Neurol 2012, 306: 685-696.CrossRef
Metadata
Title
Biomechanical and functional variation in rat sciatic nerve following cuff electrode implantation
Authors
Stephen M Restaino
Erkinay Abliz
Kelliann Wachrathit
Victor Krauthamer
Sameer B Shah
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of NeuroEngineering and Rehabilitation / Issue 1/2014
Electronic ISSN: 1743-0003
DOI
https://doi.org/10.1186/1743-0003-11-73

Other articles of this Issue 1/2014

Journal of NeuroEngineering and Rehabilitation 1/2014 Go to the issue

Research

Assessment of hand kinematics using inertial and magnetic sensors

Methodology

Manipulation of visual biofeedback during gait with a time delayed adaptive Virtual Mirror Box

Research

Stabilometric assessment of context dependent balance recovery in persons with multiple sclerosis: a randomized controlled study

Research

Association between toe flexor strength and spatiotemporal gait parameters in community-dwelling older people

Research

Effects of contralesional robot-assisted hand training in patients with unilateral spatial neglect following stroke: a case series study

Research

The potential use of spectral electromyographic fatigue as a screening and outcome monitoring tool of sarcopenic back muscle alterations