Emergence of Epidural Electrical Stimulation to Facilitate Sensorimotor Network Functionality After Spinal Cord Injury.
Originally published in Neuromodulation Journal. 2019; 22: 244-252. Traducción: Juan Carlos Andreani.
DOI:
https://doi.org/10.47924/neurotarget202179Keywords:
epidural electrical stimulation, motor-evoked responses, neuromodulation, spinal cord injury, spinal cord stimulationAbstract
Background: Traumatic spinal cord injury (SCI) disrupts signaling pathways between the brain and spinal networks below the level of injury. In cases of severe SCI, permanent loss of sensorimotor and autonomic function can occur. The standard of care for severe SCI uses compensation strategies to maximize independence during activities of daily living while living with chronic SCI-related dysfunctions. Over the past several years, the research eld of spinal neuromodulation fi has generated promising results that hold potential to enable recovery of translational research efforts that led to the emergence of EES of functions via epidural electrical stimulation (EES).
Methods: This review provides a historical account of the the spinal cord to enable intentional control of motor functions that were lost after SCI. We also highlight the major limitations associated with EES after SCI and propose future directions of spinal neuromodulation research.
Results: Multiple, independent studies have demonstrated return of motor function via EES in individuals with chronic SCI. These enabled motor functions include intentional, controlled movement of previously paralyzed extremities, independent standing and stepping, and increased grip strength. In addition, improvements in cardiovascular health, respiratory function, body composition, and urologic function have been reported.
Conclusions: EES holds promise to enable functions thought to be permanently lost due to SCI. However, EES is currently restricted to scientific investigation in humans with SCI and requires further validation of factors such as safety and efficacy before clinical translation.
Metrics
References
Kumar R, Lim J, Mekary RA et al. Traumatic spinal injury: global epidemiology and worldwide volume. World Neurosurg. 2018; 113: e345–e363. https://doi.org/10.1016/j.wneu.2018.02.033.
Simpson LA, Eng JJ, Hsieh JTC, Wolfe DL, Spinal Cord Injury Rehabilitation Evidence Scire Research Team. The health and life priorities of individuals with spinal cord injury: a systematic review. J Neurotrauma. 2012; 29: 1548-1555. https://doi.org/10.1089/neu.2011.2226.
Castro MJ, Apple DF, Rogers S, Dudley GA. Influence of complete spinal cord injury on skeletal muscle mechanics within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. 2000; 81:128–131. https://doi.org/10.1007/PL00013785.
Flank P, Wahman K, Levi R, Fahlström M. Prevalence of risk factors for cardiovascular diseases tratified by body mass index categories in patients with wheelchairdependent paraple-gia after spinal cord injury. J Rehabil Med. 2012;44:440-443. https://doi.org/10.2340/16501977-0964.
Sisto SA, Lorenz DJ, Hutchinson K, Wenzel L, Harkema SJ, Krassioukov A. Cardiovascular status of individuals with incomplete spinal cord injury from 7 neurorecovery network rehabilitation centers. Arch Phys Med Rehabil. 2012;93:1578-1587. https://doi.org/10.1016/j.apmr.2012.04.033.
Theisen D. Cardiovascular determinants of exercise capacity in the Paralympic athlete with spinal cord injury. Exp Physiol. 2012; 97:319-324. https:// doi.org/10.1113/expphysiol.2011.063016.
Moore CD, Craven BC, Thabane L et al. Lowerextremity muscle atrophy and fat infiltration after chronic spinal cord injury. J Musculoskelet Neuronal Interact. 2015;15:3241. https://doi.org/10.1016/j.jmpt.2016.02.012.
Bauman WA, Spungen AM. Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord. 2008; 46:466-476. https://doi.org/10.1038/sj.sc.3102161.
Groah SL, Nash MS, Ward EA, et al. Cardiometabolic risk in community-dwelling persons with chronic spinal cord injury. J Cardiopulm Rehabil Prev. 2011;31:73-80. https://doi.org/10.1097/HCR.0b013e3181f68a ba.
Craig A, Tran Y, Guest R et al. Psychological impact of injuries sustained in motor vehicle crashes: systematic review and meta-analysis. BMJ Open 2016;6: e011993. https://doi.org/10.1136/bmjopen-2016-011993.
Fehlings MG, Tetreault LA, Wilson JR et al. A clinical practice guideline for the management of acute spinal cord injury: introduction, rationale, and scope. Global Spine J 2017;7:84S–94S. https://doi.org/10.1177/2192568217703387.
Behrman AL, Harkema SJ. Physical rehabilitation as an agent for recovery after spinal cord injury. Phys Med Rehabil Clin N Am. 2007;18:183-202. https://doi.org/10.1016/j.pmr.2007.02.002.
Kirshblum S, Waring W. Updates for the international standards for neurological classification of spinal cord injury. Phys Med Rehabil Clin N Am. 2014; 25:505–517. https://doi.org/10.1016/j.pmr.2014.04.001.
Roberts TT, Leonard GR, Cepela DJ. Classifications in brief: American spinal injury association (ASIA) impairment scale. Clin Orthop Relat Res 2017;475:1499–1504. https://doi.org/10.1007/s11999-016-5133-4.
Field-Fote EC, Roach KE. Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial. Phys Ther 2011;91:48–60. https://doi.org/10.2522/ptj.20090359.
Harkema SJ, Schmidt-Read M, Lorenz DJ, Edgerton VR, Behrman AL. Balance and ambulation improvements in individuals with chronic incomplete spinal cord injury using locomotor trainingbased rehabilitation. Arch Phys Med Rehabil 2012;93:1508–1517. https://doi.org/10.1016/j.apmr.2011.01.024.
Forrest GF, Sisto SA, Barbeau H, et al. Neuromotor and musculoskeletal responses to locomotor training for an individual with chronic motor complete AIS-B spinal cord injury. J Spinal Cord Med 2008;31:509–521.
Dobkin B, Apple D, Barbeau H, et al. Weightsupported treadmill vs over-ground training for walking after acute incomplete SCI. Neurology 2006;66:484–492. https://doi.org/10.1212/01.wnl.0000202600.72 018.39.
Shealy CN, Mortimer JT, Reswick JB. Electrical inhibition of pain by stimulation of the dorsal columns: preliminary clinical report. Anesth Analg 1967;46:489-491. https://doi.org/10.1111/j.14698749.2009.0329 3.x.
Mekhail N, Visnjevac O, Azer G, Mehanny DS, Agrawal P, Foorsov V. Spinal cord stimulation 50 years later: clinical outcomes of spinal cord stimulation based on randomized clinical trials - a systematic review. Reg Anesth Pain Med 2018;43: 391–406. https://doi.org/10.1097/AAP.00000000000007 44.
Hussain A, Erdek M. Interventional pain management for failed back surgery syndrome. Pain Pract 2014;14:64–78. https://doi.org/10.1111/papr.12035.
Izenberg A, Perkins BA, Bril V. Diabetic neuropathies. Semin Neurol 2015;35:424-430. https://doi.org/10.1055/s-0035-1558972.
Dua A, Lee CJ. Epidemiology of peripheral arterial disease and critical limb ischemia. Tech Vasc Interv Radiol 2016;19:91-95. https://doi.org/10.1053/j.tvir.2016.04.001.
Brown TG. The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B Biol Sci. 1911;84:308-319. https://doi.org/10.1098/rspb.1911.0077.
Jankowska E, Jukes MG, Lund S, Lundberg A. The effect of DOPA on the spinal cord. 5. Reciprocal organization of pathways transmittting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 1967;70:369–388. https://doi.org/10.1111/j.17481716.1967.tb036 36.x.
Grillner S, Zangger P. How detailed is the central pattern generation for locomotion? Brain Res 1975;88:367–371. https://doi.org/10.1016/0006-8993(75)904011.
Grillner S, Rossignol S. On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 1978;146:269–277. https://doi.org/10.1016/0006-8993(78)90973-3.
Iwahara T, Atsuta Y, Garcia-Rill E, Skinner RD. Spinal cord stimulation-induced locomotion in the adult cat. Brain Res Bull 1992;28:99-105. https://doi.org/10.1016/03619230(92)90235-P.
Bussel B, Roby-Brami A, Néris OR, Yakovleff A. Evidence for a spinal stepping generator in man. Electrophysiological study. Acta Neurobiol Exp. 1996;56:465-468. https://doi.org/10.1038/sc.1996.15.
Dimitrijevic MR, Gerasimenko Y, Pinter MM. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 1998;860:360– 376. https://doi.org/10.1111/j.17496632.1998.tb090 62.x.
Minassian K, Jilge B, Rattay F et al. Steppinglike movements in humans with complete spinal cord injury induced by epidural stimulation of the lumbar cord: electromyographic study of compound muscle action potentials. Spinal Cord 2004;42:401– 416. https://doi.org/10.1038/sj.sc.3101615.
Jilge B, Minassian K, Rattay F, Dimitrijevic MR. Frequency-dependent selection of alternative spinal pathways with common periodic sensory input. Biol Cybern 2004;91:359–376. https://doi.org/10.1007/s00422-004-0511-5.
Hofstoetter US, Danner SM, Freundl B et al. Periodic modulation of repetitively elicited monosynaptic reflexes of the human lumbosacral spinal cord. J Neurophysiol 2015; 114:400–410. https://doi.org/10.1152/jn.00136.2015.
Minassian K, Persy I, Rattay F, Pinter MM, Kern H, Dimitrijevic MR. Human lumbar cord circuitries can be activated by extrinsic tonic input to generate locomotor-like activity. Hum Mov Sci 2007;26:275–295. https://doi.org/10.1016/j.humov.2007.01.005.
Danner SM, Hofstoetter US, Freundl B et al. Human spinal locomotor control is based on flexibly organized burst generators. Brain 2015;138:577-588. https://doi.org/10.1093/brain/awu372.
Minassian K, Hofstoetter US, Danner SM et al. Mechanisms of rhythm generation of the human lumbar spinal cord in response to tonic stimulation without and with step-related sensory feedback. Biomed Tech 2013;58:9–10. https://doi.org/10.1515/bmt-2013-4013.
Herman R, He J, D’Luzansky S, Willis W, Dilli S. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured. Spinal Cord 2002;40:65–68. https://doi.org/10.1038/sj.sc.3101263.
Carhart MR, He J, Herman R, D’Luzansky S, Willis WT. Epidural spinal-cord stimulation facilitates recovery of functional walking following incomplete spinal cord injury. IEEE Trans Neural Syst Rehabil Eng 2004;12:32–42. https://doi.org/10.1109/TNSRE.2003.822763.
Harkema S, Gerasimenko Y, Hodes J et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 2011;377: 1938–1947. https://doi.org/10.1016/S01406736(11)605473.
Angeli CA, Edgerton VR, Gerasimenko YP, Harkema SJ. Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans. Brain 2014;137:1394–1409. https://doi.org/10.1093/brain/awu038.
Rejc E, Angeli C, Harkema S. Effects of lumbosacral spinal cord epidural stimulation for standing after chronic complete paralysis in humans. PLoS One 2015;10:1–20. https://doi.org/10.1371/journal.pone.0133998.
Rejc E, Angeli CA, Bryant N, Harkema SJ. Effects of stand and step training with epidural stimulation on motor function for standing in chronic complete paraplegics. J Neurotrauma 2017;34:1787–1802. https://doi.org/10.1089/neu.2016.4516.
Rejc E, Angeli CA, Atkinson D, Harkema SJ. Motor recovery after activity-based training with spinal cord epidural stimulation in a chronic motor complete paraplegic. Sci Rep 2017; 7:13476. https://doi.org/10.1038/s41598-017-14003-w.
Grahn PJ, Lavrov IA, Sayenko DG et al. Enabling task-specific volitional motor functions via spinal cord neuromodulation in a human with paraplegia. Mayo Clin Proc. 2017; 92:544–554. https://doi.org/10.1016/j.mayocp.2017.02.014.
Gill ML, Grahn PJ, Calvert JS et al. Neuromodulation of lumbosacral spinal networks enables independent stepping after complete paraplegia. Nat Med. 2018; 24:16771682. https://doi.org/10.1038/s41591-0180175-7.
Calvert JS, Grahn P, Strommen J, et al. Electrophysiological guidance of epidural electrode array implantation over the human lumbosacral spinal cord to enable motor function after chronic paralysis. J Neurotrauma 2018;310:1–30. https:// doi.org/10.1089/neu.2018.5921.
Taccola G, Sayenko D, Gad P, Gerasimenko Y, Edgerton VR. And yet it moves: recovery of volitional control after spinal cord injury. Prog Neurobiol 2018;160: 64–81. https://doi.org/10.1016/j.pneurobio.2017.10.0 04.
Angeli CA, Boakye M, Morton RA et al. Recovery of over-ground walking after chronic motor complete spinal cord injury. N Engl J Med 2018;379:1244–1250. https://doi.org/10.1056/NEJMoa1803588.
Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F. Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord. 2004; 42:526–532. https://doi.org/10.1038/sj.sc.3101638.
Lu DC, Edgerton VR, Modaber M, et al. Engaging cervical spinal cord networks to reenable volitional control of hand function in tetraplegic patients. Neurorehabil Neural Repair 2016; 30:951–962. https://doi.org/10.1177/1545968316644344.
Sunshine MD, Cho FS, Lockwood DR, Fechko AS, Kasten MR, Moritz CT. Cervical intraspinal microstimulation evokes robust forelimb movements before and after injury. J Neural Eng. 2013; 10:036001. https://doi.org/10.1088/17412560/10/3/03600 1.
Alam M, Garcia-Alias G, Shah PK et al. Evaluation of optimal electrode configurations for epidural spinal cord stimulation in cervical spinal cord injured rats. J Neurosci Methods. 2015; 247:50–57. https://doi.org/10.1016/j.jneumeth.2015.03.01 2.
Alam M, Garcia-Alias G, Jin B et al. Electrical neuromodulation of the cervical spinal cord facilitates forelimb skilled function recovery in spinal cord injured www.neuromodulationjournal.com © 2019 International Neuromodulation Society Neuromodulation 2019; 22: 244–252 CALVERT ET AL. rats. Exp Neurol 2017;291:141–150. https://doi.org/10.1016/j.expneurol.2017.02.00 6.
Dimitrijevic MR, Dimitrijevic MM, Faganel J, Sherwood AM. Suprasegmentally induced motor unit activity in paralyzed muscles of patients with established spinal cord injury. Ann Neurol. 1984;16:216–221. https://doi.org/10.1002/ana.410160208.
Sherwood AM, Dimitrijevic MR, Barry MKW. Evidence of subclinical brain influence in clinically complete spinal cord injury: discomplete SCI. J Neurol Sci. 1992; 110:90– 98. https://doi.org/10.1016/0022510X(92)90014C.
Moss CW, Kilgore KL, Peckham PH. A novel command signal for motor neuroprosthetic control. Neurorehabil Neural Repair. 2011; 25:847–854. https://doi.org/10.1177/1545968311410067.
Kakulas BA. Pathology of spinal injuries. Cent Nerv Syst Trauma. 1984; 1:117–129. http://www.ncbi.nlm.nih.gov/pubmed/6545680.
Courtine G, Roy RR, Raven J, et al. Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta). Brain 2005;128:2338–2358. https://doi.org/10.1093/brain/awh604.
Rosenzweig ES, Courtine G, Jindrich DL et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 2010; 13:1505–1512. https://doi.org/10.1038/nn.2691.
Friedli L, Rosenzweig ES, Barraud Q et al. Pronounced species divergence in corticospinal tract reorganization and functional recovery after lateralized spinal cord injury favors primates. Sci Transl Med 2015;7:302ra134. https://doi.org/10.1126/scitranslmed.aac5811.
Courtine G, Song B, Roy RR et al. Recovery of supraspinal control of stepping via indirect propriospinal relay connections after spinal cord injury. Nat Med 2008;14:69–74. https://doi.org/10.1038/nm1682.
Gerasimenko Y, Musienko P, Bogacheva I et al. Propriospinal bypass of the serotonergic system that can facilitate stepping. J Neurosci 2009;29:5681–5689. https://doi.org/10.1523/JNEUROSCI.605808.2009.
Asboth L, Friedli L, Beauparlant J et al. Cortico-reticulo-spinal circuit reorganization enables functional recovery after severe spinal cord contusion. Nat Neurosci. 2018; 21:576– 588. https://doi.org/10.1038/s41593-018-0093-5.
Gerasimenko YP, Avelev VD, Nikitin OA, Lavrov IA. Initiation of locomotor activity in spinal cats by epidural stimulation of the spinal cord. Neurosci Behav Physiol. 2003; 33:247– 254. http://www.ncbi.nlm.nih.gov/pubmed/127625 91.
Gerasimenko YP, Lavrov IA, Bogacheva IN, Shcherbakova NA, Kucher VI, Musienko PE. Formation of locomotor patterns in decerebrate cats in conditions of epidural stimulation of the spinal cord. Neurosci Behav Physiol 2005;35: 291–298. https://doi.org/10.1007/s11055-005-0059-4.
Martinez M, Delivet-Mongrain H, Leblond H, Rossignol S. Effect of locomotor training in completely spinalized cats previously submitted to a spinal hemisection. J Neurosci 2012;32:10961–10970. https://doi.org/10.1523/JNEUROSCI.157812. 2012.
Merkulyeva N, Veshchitskii A, Gorsky O et al. Distribution of spinal neuronal networks controlling forward and backward locomotion. J Neurosci 2018;38:2951–2917. https://doi.org/10.1523/JNEUROSCI.295117.2018.
Ichiyama RM, Gerasimenko YP, Zhong H, Roy RR, Edgerton VR. Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation. Neurosci Lett 2005;383:339–344. https://doi.org/10.1016/j.neulet.2005.04.049.
Gerasimenko YP, Ichiyama RM, Lavrov IA et al. Epidural spinal cord stimulation plus quipazine administration enable stepping in complete spinal adult rats. J Neurophysiol 2007;98:2525–2536. https://doi.org/10.1152/jn.00836.2007.
Ichiyama RM, Gerasimenko Y, Jindrich DL, Zhong H, Roy RR, Edgerton VR. Dose dependence of the 5-HT agonist quipazine in facilitating spinal stepping in the rat with epidural stimulation. Neurosci Lett 2008;438:281–285. https://doi.org/10.1016/j.neulet.2008.04.080.
Courtine G, Gerasimenko Y, van den Brand R et al. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 2009;12:1333–1342. https://doi.org/10.1038/nn.2401.
Musienko P, van den Brand R, Marzendorfer O et al. Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J Neurosci. 2011; 31:9264–9278. https://doi.org/10.1523/JNEUROSCI.579610.2011.
Gerasimenko YP, Lavrov IA, Courtine G et al. Spinal cord reflexes induced by epidural spinal cord stimulation in normal awake rats. J Neurosci Methods. 2006; 157:253–263. https://doi.org/10.1016/j.jneumeth.2006.05.00 4.
Capogrosso M, Wenger N, Raspopovic S et al. A computational model for epidural electrical stimulation of spinal sensorimotor circuits. J Neurosci. 2013; 33:19326–19340. https://doi.org/10.1523/JNEUROSCI.168813. 2013.
Lavrov I, Dy CJ, Fong AJ, et al. Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J Neurosci. 2008; 28:6022–6029. https:// doi.org/10.1523/JNEUROSCI.0080-08.2008.
Gad P, Lavrov I, Shah P et al. Neuromodulation of motor-evoked potentials during stepping in spinal rats. J Neurophysiol 2013;110:1311– 1322. https://doi.org/10.1152/jn.00169.2013.
Cuellar CA, Mendez AA, Islam R, et al. The role of functional neuroanatomy of the lumbar spinal cord in effect of epidural stimulation. Front Neuroanat. 2017; 11:82. https://doi.org/10.3389/fnana.2017.00082.
Lavrov I, Courtine G, Dy CJ, et al. Facilitation of stepping with epidural stimulation in spinal rats: role of sensory input. J Neurosci. 2008; 28:7774–7780. https://doi.org/10.1523/JNEUROSCI.106908.2008.
Lavrov I, Gerasimenko Y, Burdick J, Zhong H, Roy RR, Edgerton VR. Integrating multiple sensory systems to modulate neural networks controlling posture. J Neurophysiol. 2015; 114: 3306-3314. https://doi.org/10.1152/jn.00583.2015.
Rattay F, Minassian K, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 2. quantitative analysis by computer modeling. Spinal Cord 2000;38:473–489. https://doi.org/10.1038/sj.sc.3101040.
Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol 1997;77:797–811. https://doi.org/10.1152/jn.1997.77.2.797.
Beauparlant J, Van Den Brand R, Barraud Q et al. Undirected compensatory plasticity contributes to neuronal dysfunction after severe spinal cord injury. Brain 2013; 136:3347–3361. https://doi.org/10.1093/brain/awt204.
Gerasimenko Y, Gorodnichev R, Moshonkina T, Sayenko D, Gad P, Reggie EV. Transcutaneous electrical spinal-cord stimulation in humans. Ann Phys Rehabil Med 2015;58:225–231. https://doi.org/10.1016/j.rehab.2015.05.003.
Gerasimenko YP, Lu DC, Modaber M et al. Noninvasive reactivation of motor descending control after paralysis. J Neurotrauma 2015;32:1968-1980. https://doi.org/10.1089/neu.2015.4008.
Rath M, Vette AH, Ramasubramaniam S, et al. Trunk stability enabled by noninvasive spinal electrical stimulation after spinal cord injury. J Neurotrauma. 2018; 35:2540–2553. https://doi.org/10.1089/neu.2017.5584.
Gad P, Lee S, Terrafranca N et al. Noninvasive activation of cervical spinal networks after severe paralysis. J Neurotrauma. 2018; 949: neu.2017.5461. https://doi.org/10.1089/neu.2017.5461.
Minassian K, Hofstoetter US, Danner SM et al. Spinal rhythm generation by step-induced feedback and transcutaneous posterior root stimulation in complete spinal cord-injured individuals. Neurorehabil Neural Repair. 2016; 30:233–243. https://doi.org/10.1177/1545968315591706.
Hofstoetter US, Krenn M, Danner SM, et al. Augmentation of voluntary locomotor activity by transcutaneous spinal cord stimulation in motor-incomplete spinal cord-injured individuals. Artif Organs 2015;39:E176–E186. https://doi.org/10.1111/aor.12615.
Sayenko DG, Angeli C, Harkema SJ, Edgerton VR, Gerasimenko YP. Neuromodulation of evoked muscle potentials induced by epidural spinal cord stimulation in paralyzed individuals. J Neurophysiol 2014;111:1088– 1099. https://doi.org/10.1152/jn.00489.2013.
Sayenko DG, Atkinson DA, Dy CJ et al. Spinal segment-specific transcutaneous stimulation differentially shapes activation pattern among motor pools in humans. J Appl Physiol 2015;118:1364–1374. https://doi.org/10.1152/japplphysiol.01128.20 14.
Ladenbauer J, Minassian K, Hofstoetter US, Dimitrijevic MR, Rattay F. Stimulation of the human lumbar spinal cord with implanted and surface electrodes: a computer simulation study. IEEE Trans Neural Syst Rehabil Eng 2010;18:637–645. https://doi.org/10.1109/TNSRE.2010.2054112
Hofstoetter US, Freundl B, Binder H, Minassian K. Common neural structures activated by epidural and transcutaneous lumbar spinal cord stimulation: elicitation of posterior root-muscle reflexes. PLoS One 2018;13:e0192013. https://doi.org/10.1371/journal.pone.0192013.
Krassioukov A, Eng JJ, Warburton DE, Teasell R. Spinal cord injury rehabilitation evidence research team. A systematic review of the management of orthostatic hypotension after spinal cord injury. Arch Phys Med Rehabil 2009;90:876–885. https://doi.org/10.1016/j.apmr.2009.01.009.
Harkema SJ, Wang S, Angeli CA, et al. Normalization of blood pressure with spinal cord epidural stimulation after severe spinal cord injury. Front Hum Neurosci. 2018; 12:1– 11. https://doi.org/10.3389/fnhum.2018.00083.
Aslan SC, Legg Ditterline BE, Park MC, et al. Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injuryinduced cardiovascular deficits. Front Physiol. 2018; 9:1–11. https://doi.org/10.3389/fphys.2018.00565.
Harkema SJ, Legg Ditterline B, Wang S, et al. Epidural spinal cord stimulation training and sustained recovery of cardiovascular function in individuals with chronic cervical spinal cord injury. JAMA Neurol. 2018; 89:3–5. https://doi.org/10.1001/jamaneurol.2018.2617.
Terson de Paleville DGL, Harkema SJ, Angeli CA. Epidural stimulation with locomotor training improves body composition in individuals with cervical or upper thoracic motor complete spinal cord injury: a series of case studies. J Spinal Cord Med 2018;0(0):1–7. doi:https://doi.org/10.1080/10790268.2018.14 49373, 42.
DiMarco AF, Kowalski KE, Geertman RT et al. Lower thoracic spinal cord stimulation to restore cough in patients with spinal cord injury: results of a National Institutes of Health-sponsored clinical trial. Part II: clinical outcomes. Arch Phys Med Rehabil. 2009; 90:726–732. https://doi.org/10.1016/j.apmr.2008.11.014.
DiMarco AF, Kowalski KE, Geertman RT, et al. Lower thoracic spinal cord stimulation to restore cough in patients with spinal cord injury: results of a National Institutes of Health-sponsored clinical trial. Part II: clinical outcomes. Arch Phys Med Rehabil. 2009; 90:726–732. https://doi.org/10.1016/j.apmr.2008.11.014.
Hachmann JT, Calvert JS, Grahn PJ, Drubach DI, Lee KH, Lavrov IA. Review of epidural spinal cord stimulation for augmenting cough after spinal cord injury. Front Hum Neurosci. 2017; 11:144. https://doi.org/10.3389/fnhum.2017.00144.
DiMarco AF, Takaoka Y, Kowalski KE. Combined intercostal and diaphragm pacing to provide artificial ventilation in patients with tetraplegia. Arch Phys Med Rehabil. 2005; 86:1200–1207. https://doi.org/10.1016/j.apmr.2004.11.027.
Hachmann JT, Grahn PJ, Calvert JS, Drubach DI, Lee KH, Lavrov IA. Electrical neuromodulation of the respiratory system after spinal cord injury. Mayo Clin Proc 2017; 92:1401–1414. https://doi.org/10.1016/j.mayocp.2017.04.011.
Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 2004;21:1371–1383. https://doi.org/10.1089/neu.2004.21.1371.
Wheeler TL, de Groat W, Eisner K, et al. Translating promising strategies for bowel and bladder management in spinal cord injury. Exp Neurol. 2018;306:169–176. https://doi.org/10.1016/j.expneurol.2018.05.00 6. www.neuromodulationjournal.com © 2019 International Neuromodulation Society Neuromodulation. 2019; 22: 244–252 EPIDURAL STIMULATION ENABLED MOTOR FUNCTION
Pettigrew RI, Heetderks WJ, Kelley CA, et al. Epidural spinal stimulation to improve bladder, bowel, and sexual function in individuals with spinal cord injuries: a framework for clinical research. IEEE Trans Biomed Eng. 2017; 64:253–262. https://doi.org/10.1109/TBME.2016.2637301.
Gad PN, Roy RR, Zhong H, Lu DC, Gerasimenko YP, Edgerton VR. Initiation of bladder voiding with epidural stimulation in paralyzed, step trained rats. PLoS One. 2014; 9:e108184. https://doi.org/10.1371/journal.pone.0108184.
Gad PN, Roy RR, Zhong H, Gerasimenko YP, Taccola G, Edgerton VR. Neuromodulation of the neural circuits controlling the lower urinary tract. Exp Neurol. 2016; 285:182–189. https://doi.org/10.1016/j.expneurol.2016.06.03 4.
Gad PN, Kokikian N, Christe KL, Edgerton VR, Havton LA. Noninvasive neurophysiological mapping of the lower urinary tract in adult and aging rhesus macaques. J Neurophysiol. 2018; 119:1521–1527. https://doi.org/10.1152/jn00840
Herrity AN, Williams CS, Angeli CA, Harkema SJ, Hubscher CH. Lumbosacral spinal cord epidural stimulation improves voiding function after human spinal cord injury. Sci Rep. 2018; 8:8688. https://doi.org/10.1038/s41598-018-26602-2.
Sim FH, Svien HJ, Bickel WH, Janes JM. Swan neck deformity following extensive cervical laminectomy. A review of twenty-one cases. J Bone Joint Surg Ser A. 1974; 56:564– 580. https://doi.org/10.2106/00004623197456030-00014.
Guigui P, Benoist M, Deburge A. Spinal deformity and instability after multilevel cervical laminectomy for spondylotic myelopathy. Spine. 1998; 23:440–447. https://doi.org/10.1097/00007632-19980215000006.
Chahoud J, Kanafani Z, Kanj SS. Surgical site infections following spine surgery: eliminating the controversies in the diagnosis. Front Med 2014; 1:7 https://doi.org/10.3389/fmed.2014.00007.
Hardman J, Graf O, Kouloumberis PE, Gao W, Chan M, Roitberg BZ. Clinical and functional outcomes of laminoplasty and laminectomy. Neurol Res. 2010; 32:416–420. https://doi.org/10.1179/174313209X459084.
Minev IR, Musienko P, Hirsch A, et al. Electronic dura mater for long-term multimodal neural interfaces. Science (80-). 2015; 347:159–163. doi:https://doi.org/10. 1126/science.1260318.
Capogrosso M, Gandar J, Greiner N, et al. Advantages of soft subdural implants for the delivery of electrochemical neuromodulation therapies to the spinal cord. J Neural Eng. 2018; 15:026024. https://doi.org/10.1088/1741-2552/aaa87a.
Formento E, Minassian K, Wagner F, et al. Electrical spinal cord stimulation must preserve proprioception to enable locomotion in humans with spinal cord injury. Nat Neurosci. 2018; 21:1728–1741. https://doi.org/10.1038/s41593-018-0262-6.
Wagner FB, Mignardot J, Le Goff-Mignardot CG, et al. Targeted neurotechnology restores walking in humans with spinal cord injury. Nature. 2018; 563:65–71. https://doi.org/10.1038/s41586-018-0649-2.
Moritz CT. Now is the critical time for engineered neuroplasticity. Neurotherapeutics. 2018; 15:628–634. https://doi.org/10.1007/s13311-018 0637-0.
Wenger N, Moraud EM, Raspopovic S, et al. Closed-loop neuromodulation of spinal sensorimotor circuits controls refined locomotion after complete spinal cord injury. Sci Transl Med. 2014; 6:255ra133. https://doi.org/10.1126/scitranslmed.3008325.
Moraud EM, Von Zitzewitz J, Miehlbradt J, et al. Closed-loop control of trunk posture improves locomotion through the regulation of leg proprioceptive feedback after spinal cord injury. Sci Rep 2018; 8:1–12. https://doi.org/10.1038/s41598-017-18293-y.
Grahn PJ, Mallory GW, Michael Berry B, Hachmann JT, Lobel DA, Luis LJ. Restoration of motor function following spinal cord injury via optimal control of intraspinal microstimulation: toward a next generation closed-loop neural prosthesis. Front Neurosci. 2014;8:1-12. https://doi.org/10.3389/fnins.2014.00296.
Dominici N, Keller U, Vallery H, et al. Versatile robotic interface to evaluate, enable and train locomotion and balance after neuromotor disorders. Nat Med. 2012; 18:1142–1147. https://doi.org/10.1038/nm.2845.
Mignardot JB, LeGoff CG, Van Den Brand R, et al. Amultidirectional gravity-assist algorithm that enhances locomotor control in patients with stroke or spinal cord injury. Sci TranslMed. 2017; 9:eaah3621. https://doi.org/10.1126/scitranslmed.aah3621.
Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Weight-bearing hindlimb stepping in treadmill-exercised adult spinal cats. Brain Res. 1990; 514:206–218. https://doi. org/10.1016/0006-8993(90)91417-F.
Lovely RG, Gregor RJ, Roy RR, Edgerton VR. Effects of training on the recovery of fullweight-bearing stepping in the adult spinal cat. Exp Neurol 1986; 92:421–435. https://doi.org/10.1016/0014-4886(86)900944.
De Leon RD, Hodgson JA, Roy RR, Edgerton VR. Retention of hindlimb stepping ability in adult spinal cats after the cessation of step training. J Neurophysiol. 1999; 81:85–94. https://doi.org/10.1152/jn.1999.81.1.85.
Shah PK, Gerasimenko Y, Shyu A, et al. Variability in step training enhances locomotor recovery after a spinal cord injury. Eur J Neurosci. 2012; 36: 2054–2062. https://doi.org/10.1111/j.14609568.2012.0810 6.x.
Behrman AL, Bowden MG, Nair PM. Neuroplasticity after spinal cord injury and training: an emerging paradigm shift in rehabilitation and walking recovery. Phys Ther 2006; 86:1406–1425. https://doi.org/10.2522/ptj.20050212.
Behrman AL, Harkema SJ. Locomotor training after human spinal cord injury: a series of case studies. Phys Ther. 2000; 80:688–700. http://www.ncbi.nlm.nih.gov/pubmed/108691 31.
Taylor-Schroeder S, LaBarbera J, McDowell S, et al. Physical therapy treatment time during inpatient spinal cord injury rehabilitation. J Spinal Cord Med. 2011; 34:149–161. https://doi.org/10.1179/107902611X12971826 988057.
Steele SS. Sacral nerve stimulation: 50 years in the making. Can Urol Assoc J. 2012; 6:231– 232. https://doi.org/10.5489/cuaj.12194.
Youngerman BE, Chan AK, Mikell CB, McKhann GM, Sheth SA. A decade of emerging indications: deep brain stimulation in the United States. J Neurosurg. 2016; 125:461– 471. https://doi.org/10.3171/2015.7.JNS142599.
Fins JJ, Mayberg HS, Nuttin B, et al. Analysis & commentary: misuse of the FDA’s humanitarian device exemption in deep brain stimulation for obsessive-compulsive disorder. Health Aff. 2011; 30: 302311. https://doi.org/10.1377/hlthaff.2010.0157.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 2021
This work is licensed under a Creative Commons Attribution 4.0 International License.
The article is distributed under the Creative Commons Attribution 4.0 License. Unless otherwise stated, associated published material is distributed under the same licence.