From Trial to Chronic Epidural Electrical Stimulation: A Single-Patient Feasibility Study in Motor-Complete Spinal Cord Injury
Abstract
1. Introduction
2. Case Presentation
3. Results
3.1. Motor Performance with Trial Perc-EES and Paddle-EES During “Flexion–Extension” Test
3.2. Trial Perc-EES and Paddle-EES Facilitated Rhythmic Activity in Side-Lying Position
3.3. Trial Perc-EES and Paddle-EES Facilitated Rhythmic Activity in Upright Position
3.4. Clinical Assessment
4. Discussion
5. Conclusions
6. Limitations
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
| BWS | Body weight support |
| EES | Epidural electrical stimulation |
| Paddle-EES | Chronic paddle-electrodes epidural electrical stimulation |
| Perc-EES | Percutaneous-epidural electrical stimulation |
| SCI | Spinal cord injury |
| AIS | American Spinal Injury Association Impairment Scale |
| CSF | Cerebrospinal fluid |
| UTI | Urinary tract infection |
| MRI | Magnetic resonance imaging |
| EMG | Electromyography |
| AUC | Area under the curve |
| SEMP | Spinally evoked motor potential |
| BF | Biceps femoris |
| RF | Rectus femoris |
| TA | Tibialis anterior |
| GM | Medial gastrocnemius |
| VL | Vastus lateralis |
| SOL | Soleus |
| AIS | ASIA Impairment Scale |
| NLI | Neurological level of injury |
| LEMS | Lower extremity motor score |
| VAC | Voluntary anal contraction |
| DAP | Deep anal pressure |
References
- Gill, M.L.; Grahn, P.J.; Calvert, J.S.; Linde, M.B.; Lavrov, I.A.; Strommen, J.A.; Beck, L.A.; Sayenko, D.G.; Van Straaten, M.G.; Drubach, D.I.; et al. Neuromodulation of Lumbosacral Spinal Networks Enables Independent Stepping after Complete Paraplegia. Nat. Med. 2018, 24, 1677–1682. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Minassian, K.; Jilge, B.; Rattay, F.; Pinter, M.M.; Binder, H.; Gerstenbrand, F.; Dimitrijevic, M.R. Stepping-like 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. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Vaarwerk, I.A.T.; Staal, M.J. Spinal Cord Stimulation in Chronic Pain Syndromes. Spinal Cord 1998, 36, 671–682. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kumar, R.; Lozano, A.M.; Kim, Y.J.; Hutchison, W.D.; Sime, E.; Halket, E.; Lang, A.E. Double-Blind Evaluation of Subthalamic Nucleus Deep Brain Stimulation in Advanced Parkinson’s Disease. Neurology 1998, 51, 850–855. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Angeli, C.A.; Boakye, M.; Morton, R.A.; Vogt, J.; Benton, K.; Chen, Y.; Ferreira, C.K.; Harkema, S.J. Recovery of Over-Ground Walking after Chronic Motor Complete Spinal Cord Injury. N. Engl. J. Med. 2018, 379, 1244–1250. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Wagner, F.B.; Mignardot, J.-B.; Le Goff-Mignardot, C.G.; Demesmaeker, R.; Komi, S.; Capogrosso, M.; Rowald, A.; Seáñez, I.; Caban, M.; Pirondini, E.; et al. Targeted Neurotechnology Restores Walking in Humans with Spinal Cord Injury. Nature 2018, 563, 65–71. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Steadman, C.J.; Grill, W.M. Spinal Cord Stimulation for the Restoration of Bladder Function after Spinal Cord Injury. Healthc. Technol. Lett. 2020, 7, 87–92. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Barolat, G.; Myklebust, J.B.; Wenninger, W. Effects of Spinal Cord Stimulation on Spasticity and Spasms Secondary to Myelopathy. Stereotact. Funct. Neurosurg. 1988, 51, 29–44. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Angeli, C.; Rejc, E.; Boakye, M.; Herrity, A.; Mesbah, S.; Hubscher, C.; Forrest, G.; Harkema, S. Targeted Selection of Stimulation Parameters for Restoration of Motor and Autonomic Function in Individuals With Spinal Cord Injury. Neuromodulation J. Int. Neuromodulation Soc. 2024, 27, 645–660. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Dimitrijevic, M.M.; Dimitrijevic, M.R.; Illis, L.S.; Nakajima, K.; Sharkey, P.C.; Sherwood, A.M. Spinal Cord Stimulation for the Control of Spasticity in Patients with Chronic Spinal Cord Injury: I. Clinical Observations. Cent. Nerv. Syst. Trauma 1986, 3, 129–143. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Jilge, B.; Minassian, K.; Rattay, F.; Pinter, M.M.; Gerstenbrand, F.; Binder, H.; Dimitrijevic, M.R. Initiating Extension of the Lower Limbs in Subjects with Complete Spinal Cord Injury by Epidural Lumbar Cord Stimulation. Exp. Brain Res. 2004, 154, 308–326. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Harkema, S.; Gerasimenko, Y.; Hodes, J.; Burdick, J.; Angeli, C.; Chen, Y.; Ferreira, C.; Willhite, A.; Rejc, E.; Grossman, R.G.; 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. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Gerasimenko, Y.; Gorodnichev, R.; Moshonkina, T.; Sayenko, D.; Gad, P.; Reggie Edgerton, V. Transcutaneous Electrical Spinal-Cord Stimulation in Humans. Ann. Phys. Rehabil. Med. 2015, 58, 225–231. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Gad, P.; Gerasimenko, Y.; Zdunowski, S.; Turner, A.; Sayenko, D.; Lu, D.C.; Edgerton, V.R. Weight Bearing Over-Ground Stepping in an Exoskeleton with Non-Invasive Spinal Cord Neuromodulation after Motor Complete Paraplegia. Front. Neurosci. 2017, 11, 333. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Sayenko, D.G.; Rath, M.; Ferguson, A.R.; Burdick, J.W.; Havton, L.A.; Edgerton, V.R.; Gerasimenko, Y.P. Self-Assisted Standing Enabled by Non-Invasive Spinal Stimulation after Spinal Cord Injury. J. Neurotrauma 2019, 36, 1435–1450. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Yang, B.; Zhang, F.; Cheng, F.; Ying, L.; Wang, C.; Shi, K.; Wang, J.; Xia, K.; Gong, Z.; Huang, X.; et al. Strategies and Prospects of Effective Neural Circuits Reconstruction after Spinal Cord Injury. Cell Death Dis. 2020, 11, 439. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Meyer, C.; Hofstoetter, U.S.; Hubli, M.; Hassani, R.H.; Rinaldo, C.; Curt, A.; Bolliger, M. Immediate Effects of Transcutaneous Spinal Cord Stimulation on Motor Function in Chronic, Sensorimotor Incomplete Spinal Cord Injury. J. Clin. Med. 2020, 9, 3541. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Biktimirov, A.; Bryukhovetskiy, I.; Sharma, A.; Sharma, H.S. Spinal Cord Stimulation and Intrathecal Baclofen Therapy for Patients with Severe Spasticity after Spinal Cord Injury. In Progress in Brain Research; Elsevier: Amsterdam, The Netherlands, 2020; Volume 258, pp. 79–99. [Google Scholar]
- Mukhametova, E.; Militskova, A.; Biktimirov, A.; Kharin, N.; Semenova, E.; Sachenkov, O.; Baltina, T.; Lavrov, I. Consecutive Transcutaneous and Epidural Spinal Cord Neuromodulation to Modify Clinical Complete Paralysis—The Proof of Concept. Mayo Clin. Proc. Innov. Qual. Outcomes 2024, 8, 1–16. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Solinsky, R.; Specker-Sullivan, L.; Wexler, A. Current Barriers and Ethical Considerations for Clinical Implementation of Epidural Stimulation for Functional Improvement after Spinal Cord Injury. J. Spinal Cord Med. 2020, 43, 653–656. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Wenger, N.; Moraud, E.M.; Gandar, J.; Musienko, P.; Capogrosso, M.; Baud, L.; Le Goff, C.G.; Barraud, Q.; Pavlova, N.; Dominici, N.; et al. Spatiotemporal Neuromodulation Therapies Engaging Muscle Synergies Improve Motor Control after Spinal Cord Injury. Nat. Med. 2016, 22, 138–145. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Sherwood, A.M.; Dimitrijevic, M.R.; Barry McKay, W. Evidence of Subclinical Brain Influence in Clinically Complete Spinal Cord Injury: Discomplete SCI. J. Neurol. Sci. 1992, 110, 90–98. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Militskova, A.; Mukhametova, E.; Fatykhova, E.; Sharifullin, S.; Cuellar, C.A.; Calvert, J.S.; Grahn, P.J.; Baltina, T.; Lavrov, I. Supraspinal and Afferent Signaling Facilitate Spinal Sensorimotor Network Excitability After Discomplete Spinal Cord Injury: A Case Report. Front. Neurosci. 2020, 14, 552. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Seáñez, I.; Capogrosso, M. Motor Improvements Enabled by Spinal Cord Stimulation Combined with Physical Training after Spinal Cord Injury: Review of Experimental Evidence in Animals and Humans. Bioelectron. Med. 2021, 7, 16. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Formento, E.; Minassian, K.; Wagner, F.; Mignardot, J.B.; Le Goff-Mignardot, C.G.; Rowald, A.; Bloch, J.; Micera, S.; Capogrosso, M.; Courtine, G. Electrical Spinal Cord Stimulation Must Preserve Proprioception to Enable Locomotion in Humans with Spinal Cord Injury. Nat. Neurosci. 2018, 21, 1728–1741. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Darrow, D.; Balser, D.; Netoff, T.I.; Krassioukov, A.; Phillips, A.; Parr, A.; Samadani, U. Epidural Spinal Cord Stimulation Facilitates Immediate Restoration of Dormant Motor and Autonomic Supraspinal Pathways after Chronic Neurologically Complete Spinal Cord Injury. J. Neurotrauma 2019, 36, 2325–2336. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kakulas, B.A. Pathology of Spinal Injuries. Cent. Nerv. Syst. Trauma 1984, 1, 117–126. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Nicotra, A.; Ellaway, P.H. Thermal Perception Thresholds: Assessing the Level of Human Spinal Cord Injury. Spinal Cord 2006, 44, 617–624. [Google Scholar] [CrossRef] [Scilit] [PubMed][Green Version]
- Dimitrijevic, M.R.; Dimitrijevic, M.M.; Faganel, J.; Sherwood, A.M. Suprasegmentally Induced Motor Unit Activity in Paralyzed Muscles of Patients with Established Spinal Cord Injury. Ann. Neurol. 1984, 16, 216–221. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rowland, J.W.; Hawryluk, G.W.J.; Kwon, B.; Fehlings, M.G. Current Status of Acute Spinal Cord Injury Pathophysiology and Emerging Therapies: Promise on the Horizon. Neurosurg. Focus 2008, 25, E2. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Grahn, P.J.; Lavrov, I.A.; Sayenko, D.G.; Van Straaten, M.G.; Gill, M.L.; Strommen, J.A.; Calvert, J.S.; Drubach, D.I.; Beck, L.A.; Linde, M.B.; et al. Enabling Task-Specific Volitional Motor Functions via Spinal Cord Neuromodulation in a Human With Paraplegia. Mayo Clin. Proc. 2017, 92, 544–554. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Dombovy-Johnson, M.L.; D’Souza, R.S.; Ha, C.T.; Hagedorn, J.M. Incidence and Risk Factors for Spinal Cord Stimulator Lead Migration With or Without Loss of Efficacy: A Retrospective Review of 91 Consecutive Thoracic Lead Implants. Neuromodulation Technol. Neural Interface 2022, 25, 731–737. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Zhang, T.C.; Janik, J.J.; Grill, W.M. Mechanisms and Models of Spinal Cord Stimulation for the Treatment of Neuropathic Pain. Brain Res. 2014, 1569, 19–31. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rattay, F. The Basic Mechanism for the Electrical Stimulation of the Nervous System. Neuroscience 1999, 89, 335–346. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rattay, F.; Minassian, K.; Dimitrijevic, M. Epidural Electrical Stimulation of Posterior Structures of the Human Lumbosacral Cord: 2. Quantitative Analysis by Computer Modeling. Spinal Cord 2000, 38, 473–489. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Manola, L.; Holsheimer, J.; Veltink, P. Technical Performance of Percutaneous Leads for Spinal Cord Stimulation: A Modeling Study. Neuromodulation Technol. Neural Interface 2005, 8, 88–99. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Holsheimer, J.; Wesselink, W.A. Optimum Electrode Geometry for Spinal Cord Stimulation: The Narrow Bipole and Tripole. Med. Biol. Eng. Comput. 1997, 35, 493–497. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Chadwick, R.; McNaughton, R.; Eldabe, S.; Baranidharan, G.; Bell, J.; Brookes, M.; Duarte, R.V.; Earle, J.; Gulve, A.; Houten, R.; et al. To Trial or Not to Trial Before Spinal Cord Stimulation for Chronic Neuropathic Pain: The Patients’ View From the TRIAL-STIM Randomized Controlled Trial. Neuromodulation Technol. Neural Interface 2021, 24, 459–470. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Angeli, C.A.; Edgerton, V.R.; Gerasimenko, Y.P.; Harkema, S.J. Altering Spinal Cord Excitability Enables Voluntary Movements after Chronic Complete Paralysis in Humans. Brain 2014, 137, 1394–1409. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kim, C.H.; Green, A.W.; Rodgers, D.E.; Issa, M.A.; Ata, M.A. Importance of Axial Migration of Spinal Cord Stimulation Trial Leads with Position. Pain Physician 2013, 16, E763–E768. [Google Scholar] [CrossRef] [Scilit]
- Carhart, M.R.; He, J.; Herman, R.; D’Luzansky, S.; Willis, W.T. Epidural Spinal-Cord Stimulation Facilitates Recovery of Functional Walking Following Incomplete Spinal-Cord Injury. IEEE Trans. Neural Syst. Rehabil. Eng. 2004, 12, 32–42. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Winkel, J.; Jørgensen, K. Significance of Skin Temperature Changes in Surface Electromyography. Eur. J. Appl. Physiol. 1991, 63, 345–348. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- McManus, L.; De Vito, G.; Lowery, M.M. Analysis and Biophysics of Surface EMG for Physiotherapists and Kinesiologists: Toward a Common Language With Rehabilitation Engineers. Front. Neurol. 2020, 11, 576729. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Balbinot, G.; Li, G.; Wiest, M.J.; Pakosh, M.; Furlan, J.C.; Kalsi-Ryan, S.; Zariffa, J. Properties of the Surface Electromyogram Following Traumatic Spinal Cord Injury: A Scoping Review. J. Neuroeng. Rehabil. 2021, 18, 105. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Moshonkina, T.R.; Shandybina, N.D.; Moiseev, S.A.; Grishin, A.A.; Gerasimenko, Y.P. Muscle Coactivation Phenomenon in the Modulation of Walking by Electrical Stimulation of the Spinal Cord. Hum. Physiol. 2021, 47, 175–182. [Google Scholar] [CrossRef] [Scilit]
- Carey, H.D.; De Groote, F.; Sawers, A. A Comparative Analysis of Co-Contraction Indices Using Synthetic EMG Data: Implications for Selection and Interpretation. PLoS ONE 2026, 21, e0343081. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Hales, M.; Biros, E.; Reznik, J.E. Reliability and Validity of the Sensory Component of the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI): A Systematic Review. Top. Spinal Cord Inj. Rehabil. 2015, 21, 241–249. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Negrini, S.; Imperio, G.; Villafañe, J.H.; Negrini, F.; Zaina, F. Systematic Reviews of Physical and Rehabilitation Medicine Cochrane Contents. Part 1. Disabilities Due to Spinal Disorders and Pain Syndromes in Adults. Eur. J. Phys. Rehabil. Med. 2013, 49, 597–609. [Google Scholar] [PubMed]
- Santos, J.V.; Padron-Monedero, A.; Bikbov, B.; Grad, D.A.; Plass, D.; Mechili, E.A.; Gazzelloni, F.; Fischer, F.; Sulo, G.; Ngwa, C.H.; et al. The State of Health in the European Union (EU-27) in 2019: A Systematic Analysis for the Global Burden of Disease Study 2019. BMC Public Health 2024, 24, 1374. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Herrity, A.N.; Aslan, S.C.; Mesbah, S.; Siu, R.; Kalvakuri, K.; Ugiliweneza, B.; Mohamed, A.; Hubscher, C.H.; Harkema, S.J. Targeting Bladder Function with Network-Specific Epidural Stimulation after Chronic Spinal Cord Injury. Sci. Rep. 2022, 12, 11179. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Chalif, J.I.; Chavarro, V.S.; Mensah, E.; Johnston, B.; Fields, D.P.; Chalif, E.J.; Chiang, M.; Sutton, O.; Yong, R.; Trumbower, R.; et al. Epidural Spinal Cord Stimulation for Spinal Cord Injury in Humans: A Systematic Review. J. Clin. Med. 2024, 13, 1090. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Hachmann, J.T.; Yousak, A.; Wallner, J.J.; Gad, P.N.; Edgerton, V.R.; Gorgey, A.S. Epidural Spinal Cord Stimulation as an Intervention for Motor Recovery after Motor Complete Spinal Cord Injury. J. Neurophysiol. 2021, 126, 1843–1859. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Calvert, J.S.; Grahn, P.J.; Strommen, J.A.; Lavrov, I.A.; Beck, L.A.; Gill, M.L.; Linde, M.B.; Brown, D.A.; Van Straaten, M.G.; Veith, D.D.; et al. Electrophysiological Guidance of Epidural Electrode Array Implantation over the Human Lumbosacral Spinal Cord to Enable Motor Function after Chronic Paralysis. J. Neurotrauma 2019, 36, 1451–1460. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Cuellar, C.A.; Mendez, A.A.; Islam, R.; Calvert, J.S.; Grahn, P.J.; Knudsen, B.; Pham, T.; Lee, K.H.; Lavrov, I.A. The Role of Functional Neuroanatomy of the Lumbar Spinal Cord in Effect of Epidural Stimulation. Front. Neuroanat. 2017, 11, 82. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Mendez, A.; Islam, R.; Latypov, T.; Basa, P.; Joseph, O.J.; Knudsen, B.; Siddiqui, A.M.; Summer, P.; Staehnke, L.J.; Grahn, P.J.; et al. Segment-Specific Orientation of the Dorsal and Ventral Roots for Precise Therapeutic Targeting of Human Spinal Cord. Mayo Clin. Proc. 2021, 96, 1426–1437. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Capogrosso, M.; Wagner, F.B.; Gandar, J.; Moraud, E.M.; Wenger, N.; Milekovic, T.; Shkorbatova, P.; Pavlova, N.; Musienko, P.; Bezard, E.; et al. Configuration of Electrical Spinal Cord Stimulation through Real-Time Processing of Gait Kinematics. Nat. Protoc. 2018, 13, 2031–2061. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rejc, E.; Angeli, C.A. Spinal Cord Epidural Stimulation for Lower Limb Motor Function Recovery in Individuals with Motor Complete Spinal Cord Injury. Phys. Med. Rehabil. Clin. N. Am. 2019, 30, 337–354. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Hofstoetter, U.S.; Perret, I.; Bayart, A.; Lackner, P.; Binder, H.; Freundl, B.; Minassian, K. Spinal Motor Mapping by Epidural Stimulation of Lumbosacral Posterior Roots in Humans. iScience 2021, 24, 101930. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rowald, A.; Komi, S.; Demesmaeker, R.; Baaklini, E.; Hernandez-Charpak, S.D.; Paoles, E.; Montanaro, H.; Cassara, A.; Becce, F.; Lloyd, B.; et al. Activity-Dependent Spinal Cord Neuromodulation Rapidly Restores Trunk and Leg Motor Functions after Complete Paralysis. Nat. Med. 2022, 28, 260–271. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Lam, D.V.; Chin, J.; Brucker-Hahn, M.K.; Settell, M.; Romanauski, B.; Verma, N.; Upadhye, A.; Deshmukh, A.; Skubal, A.; Nishiyama, Y.; et al. The Role of Spinal Cord Neuroanatomy in the Variances of Epidural Spinal Recordings. Bioelectron. Med. 2024, 10, 17. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Verma, N.; Romanauski, B.; Lam, D.; Lujan, L.; Blanz, S.; Ludwig, K.; Lempka, S.; Shoffstall, A.; Knudson, B.; Nishiyama, Y.; et al. Characterization and Applications of Evoked Responses during Epidural Electrical Stimulation. Bioelectron. Med. 2023, 9, 5. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Xie, F.; Bai, C.; Luan, X.; Xu, J. Research Progress on the Effects of Epidural Electrical Stimulation on Lower Extremity Function in Patients with Spinal Cord Injury. Front. Med. 2026, 13, 1861870. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Sayenko, D.G.; Angeli, C.; Harkema, S.J.; Edgerton, V.R.; Gerasimenko, Y.P. Neuromodulation of Evoked Muscle Potentials Induced by Epidural Spinal-Cord Stimulation in Paralyzed Individuals. J. Neurophysiol. 2014, 111, 1088–1099. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Heald, E.; Hart, R.; Kilgore, K.; Peckham, P.H. Characterization of Volitional Electromyographic Signals in the Lower Extremity After Motor Complete Spinal Cord Injury. Neurorehabil. Neural Repair 2017, 31, 583–591. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rudolph, K.S.; Axe, M.J.; Snyder-Mackler, L. Dynamic Stability after ACL Injury: Who Can Hop? Knee Surg. Sports Traumatol. Arthrosc. 2000, 8, 262–269. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Li, G.; Shourijeh, M.S.; Ao, D.; Patten, C.; Fregly, B.J. How Well Do Commonly Used Co-Contraction Indices Approximate Lower Limb Joint Stiffness Trends During Gait for Individuals Post-Stroke? Front. Bioeng. Biotechnol. 2021, 8, 588908. [Google Scholar] [CrossRef] [Scilit] [PubMed]




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Militskova, A.; Mukhametova, E.; Biktimirov, A.; Andrianov, V.; Yakovleva, E.; Silantyeva, D.; Lavrov, I. From Trial to Chronic Epidural Electrical Stimulation: A Single-Patient Feasibility Study in Motor-Complete Spinal Cord Injury. J. Clin. Med. 2026, 15, 6663. https://doi.org/10.3390/jcm15176663
Militskova A, Mukhametova E, Biktimirov A, Andrianov V, Yakovleva E, Silantyeva D, Lavrov I. From Trial to Chronic Epidural Electrical Stimulation: A Single-Patient Feasibility Study in Motor-Complete Spinal Cord Injury. Journal of Clinical Medicine. 2026; 15(17):6663. https://doi.org/10.3390/jcm15176663
Chicago/Turabian StyleMilitskova, Alena, Elvira Mukhametova, Artur Biktimirov, Vyacheslav Andrianov, Elena Yakovleva, Dinara Silantyeva, and Igor Lavrov. 2026. "From Trial to Chronic Epidural Electrical Stimulation: A Single-Patient Feasibility Study in Motor-Complete Spinal Cord Injury" Journal of Clinical Medicine 15, no. 17: 6663. https://doi.org/10.3390/jcm15176663
APA StyleMilitskova, A., Mukhametova, E., Biktimirov, A., Andrianov, V., Yakovleva, E., Silantyeva, D., & Lavrov, I. (2026). From Trial to Chronic Epidural Electrical Stimulation: A Single-Patient Feasibility Study in Motor-Complete Spinal Cord Injury. Journal of Clinical Medicine, 15(17), 6663. https://doi.org/10.3390/jcm15176663

