Skip to main content

Advertisement

Log in

A Review of Functional Electrical Stimulation Treatment in Spinal Cord Injury

  • Review
  • Published:
NeuroMolecular Medicine Aims and scope Submit manuscript

Abstract

Functional electrical stimulation (FES) has been widely adopted to elicit muscle contraction in rehabilitation training after spinal cord injury (SCI). Conventional FES modalities include stimulations coupled with rowing, cycling, assisted walking and other derivatives. In this review, we studied thirteen clinical reports from the past 5 years and evaluated the effects of various FES aided rehabilitation plans on the functional recovery after SCI, highlighting upper and lower extremity strength, cardiopulmonary function, and balder control. We further explored potential mechanisms of FES using the Hebbian theory and lumbar locomotor central pattern generators. Overall, FES can be used to improve respiration, circulation, hand strength, mobility, and metabolism after SCI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal, G., Sherman, D., Maybhate, A., Gorelik, M., Kerr, D. A., Thakor, N. V., et al. (2010). Slope analysis of somatosensory evoked potentials in spinal cord injury for detecting contusion injury and focal demyelination. Journal of Clinical Neuroscience, 17(9), 1159–1164. https://doi.org/10.1016/j.jocn.2010.02.005.

    Article  PubMed  Google Scholar 

  • Agrawal, G., Sherman, D., Thakor, N., & All, A. (2008). A novel shape analysis technique for somatosensory evoked potentials. In 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, 1–8, (p. 4688). https://doi.org/10.1109/Iembs.2008.4650259

  • Al-Nashash, H., Fatoo, N. A., Mirza, N. N., Ahmed, R. I., Agrawal, G., Thakor, N. V., et al. (2009). Spinal cord injury detection and monitoring using spectral coherence. IEEE Transactions on Biomedical Engineering, 56(8), 1971–1979. https://doi.org/10.1109/Tbme.2009.2018296.

    Article  PubMed  Google Scholar 

  • All, A. H., Bazley, F. A., Gupta, S., Pashai, N., Hu, C., Pourmorteza, A., et al. (2012). Human embryonic stem cell-derived oligodendrocyte progenitors aid in functional recovery of sensory pathways following contusive spinal cord injury. PLoS ONE, 7(10), e47645. https://doi.org/10.1371/journal.pone.0047645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ambrosini, E., Ferrante, S., Schauer, T., Ferrigno, G., Molteni, F., & Pedrocchi, A. (2010). Design of a symmetry controller for cycling induced by electrical stimulation: Preliminary results on post-acute stroke patients. Artificial Organs. https://doi.org/10.1111/j.1525-1594.2009.00941.x.

    Article  PubMed  Google Scholar 

  • American Spinal Injury Association. (2002). International standards for neurological classification of SCI. The Journal of Spinal Cord Medicine, 34, 535–546.

    Google Scholar 

  • Baker, L. L., Bowman, B. R., & McNeal, D. R. (1988). Effects of waveform on comfort during neuromuscular electrical stimulation. Clinical Orthopaedics and Related Research, 233, 75–85.

    Google Scholar 

  • Bakkum, A. J., de Groot, S., Stolwijk-Swuste, J. M., van Kuppevelt, D. J., van der Woude, L. H., et al. (2015). Effects of hybrid cycling versus handcycling on wheelchair-specific fitness and physical activity in people with long-term spinal cord injury: A 16-week randomized controlled trial. Spinal Cord, 53(5), 395–401. https://doi.org/10.1038/sc.2014.237.

    Article  CAS  PubMed  Google Scholar 

  • Bareyre, F. M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T. C., Weinmann, O., & Schwab, M. E. (2004). The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nature Neuroscience, 7(3), 269–277. https://doi.org/10.1038/nn1195.

    Article  CAS  PubMed  Google Scholar 

  • Bazley, F. A., All, A. H., Thakor, N. V., & Maybhate, A. (2011). Plasticity associated changes in cortical somatosensory evoked potentials following spinal cord injury in rats. In Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Embc), (pp. 2005–2008).

  • Bellman, M. J., Cheng, T. H., Downey, R. J., & Dixon, W. E. (2014). Stationary cycling induced by switched functional electrical stimulation control. In American Control Conference (Acc), (pp. 4802–4809).

  • Bergquist, A. J., Clair, J. M., Lagerquist, O., Mang, C. S., Okuma, Y., & Collins, D. F. (2011). Neuromuscular electrical stimulation: Implications of the electrically evoked sensory volley. European Journal of Applied Physiology, 111(10), 2409–2426. https://doi.org/10.1007/s00421-011-2087-9.

    Article  CAS  PubMed  Google Scholar 

  • Bersch, I., & Friden, J. (2016). Role of functional electrical stimulation in tetraplegia hand surgery. Archives of Physical Medicine and Rehabilitation, 97(6 Suppl), S154–159. https://doi.org/10.1016/j.apmr.2016.01.035.

    Article  PubMed  Google Scholar 

  • Bhadra, N., & Peckham, P. H. (1997). Peripheral nerve stimulation for restoration of motor function. Journal of Clinical Neurophysiology, 14(5), 378–393.

    CAS  PubMed  Google Scholar 

  • Bickel, C. S., Slade, J. M., VanHiel, L. R., Warren, G. L., & Dudley, G. A. (2004). Variable-frequency-train stimulation of skeletal muscle after spinal cord injury. Journal of Rehabilitation Research and Development, 41(1), 33–40.

    PubMed  Google Scholar 

  • Brindley, G. S. (1977). An implant to empty the bladder or close the urethra. Journal of Neurology, Neurosurgery and Psychiatry, 40(4), 358–369. https://doi.org/10.1136/jnnp.40.4.358.

    Article  CAS  PubMed  Google Scholar 

  • Carel, C., Loubinoux, I., Boulanouar, K., Manelfe, C., Rascol, O., Celsis, P., et al. (2000). Neural substrate for the effects of passive training on sensorimotor cortical representation: A study with functional magnetic resonance imaging in healthy subjects. Journal of Cerebral Blood Flow & Metabolism, 20(3), 478–484.

    CAS  Google Scholar 

  • Coupaud, S., Gollee, H., Hunt, K. J., Fraser, M. H., Allan, D. B., & McLean, A. N. (2008). Arm-cranking exercise assisted by Functional Electrical Stimulation in C6 tetraplegia: A pilot study. Technology and Health Care, 16(6), 415–427.

    CAS  PubMed  Google Scholar 

  • Creasey, G. H., & Craggs, M. D. (2012). Functional electrical stimulation for bladder, bowel, and sexual function. Handbook of Clinical Neurology, 109, 247–257. https://doi.org/10.1016/B978-0-444-52137-8.00015-2.

    Article  PubMed  Google Scholar 

  • Dancause, N., & Nudo, R. J. (2011). Shaping plasticity to enhance recovery after injury. Progress in Brain Research, 192, 273–295. https://doi.org/10.1016/B978-0-444-53355-5.00015-4.

    Article  PubMed  PubMed Central  Google Scholar 

  • de Kroon, J. R., IJzerman, M. J., Chae, J., Lankhorst, G. J., & Zilvold, G. (2005). Relation between stimulation characteristics and clinical outcome in studies using electrical stimulation to improve motor control of the upper extremity in stroke. Journal of Rehabilitation Medicine, 37, 65–74.

    PubMed  Google Scholar 

  • Deley, G., Denuziller, J., Babault, N., & Taylor, J. A. (2015). Effects of electrical stimulation pattern on quadriceps isometric force and fatigue in individuals with spinal cord injury. Muscle and Nerve, 52(2), 260–264. https://doi.org/10.1002/mus.24530.

    Article  PubMed  Google Scholar 

  • Dimitrijevic, M. R., Gerasimenko, Y., & Pinter, M. M. (1998). Evidence for a spinal central pattern generator in humans. Annals of the New York Academy of Sciences, 860, 360–376. https://doi.org/10.1111/j.1749-6632.1998.tb09062.x.

    Article  CAS  PubMed  Google Scholar 

  • Dobkin, B. H. (2003). Do electrically stimulated sensory inputs and movements lead to long-term plasticity and rehabilitation gains? Current Opinion in Neurology, 16(6), 685–691.

    PubMed  Google Scholar 

  • Doucet, B. M., Lam, A., & Griffin, L. (2012). Neuromuscular electrical stimulation for skeletal muscle function. The Yale Journal of Biology and Medicine, 85(2), 201–215.

    PubMed  PubMed Central  Google Scholar 

  • Downey, R. J., Bellman, M., Sharma, N., Wang, Q., Gregory, C. M., & Dixon, W. E. (2011). A novel modulation strategy to increase stimulation duration in neuromuscular electrical stimulation. Muscle and Nerve, 44(3), 382–387. https://doi.org/10.1002/mus.22058.

    Article  PubMed  Google Scholar 

  • Downey, R. J., Bellman, M. J., Kawai, H., Gregory, C. M., & Dixon, W. E. (2014). Comparing the induced muscle fatigue between asynchronous and synchronous electrical stimulation in able-bodied and spinal cord injured populations. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 23(6), 964–972.

    PubMed  Google Scholar 

  • Eser, P. C., Donaldson Nde, N., Knecht, H., & Stussi, E. (2003). Influence of different stimulation frequencies on power output and fatigue during FES-cycling in recently injured SCI people. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 11(3), 236–240. https://doi.org/10.1109/TNSRE.2003.817677.

    Article  PubMed  Google Scholar 

  • Ethier, C., Gallego, J., & Miller, L. E. (2015). Brain-controlled neuromuscular stimulation to drive neural plasticity and functional recovery. Current Opinion in Neurobiology, 33, 95–102.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fazio, C. (2014). Functional electrical stimulation for incomplete spinal cord injury. Baylor University Medical Center Proceedings, 27(4), 353–355. https://doi.org/10.1080/08998280.2014.11929157.

    Article  PubMed  Google Scholar 

  • Ferrante, S., Ambrosini, E., Ferrigno, G., & Pedrocchi, A. (2012). Biomimetic NMES controller for arm movements supported by a passive exoskeleton. In Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Embc), (pp. 1888–1891).

  • Figoni, S. F. (1990). Perspectives on cardiovascular fitness and SCI. The Journal of the American Paraplegia Society, 13(4), 63–71.

    CAS  PubMed  Google Scholar 

  • Furlan, J. C., & Fehlings, M. G. (2008). Cardiovascular complications after acute spinal cord injury: Pathophysiology, diagnosis, and management. Neurosurgical Focus. https://doi.org/10.3171/Foc.2008.25.11.E13.

    Article  PubMed  Google Scholar 

  • Gargiulo, P., Reynisson, P. J., Helgason, B., Kern, H., Mayr, W., Ingvarsson, P., et al. (2011). Muscle, tendons, and bone: Structural changes during denervation and FES treatment. Neurological Research, 33(7), 750–758. https://doi.org/10.1179/1743132811Y.0000000007.

    Article  PubMed  Google Scholar 

  • Gater, D. R., Jr., Dolbow, D., Tsui, B., & Gorgey, A. S. (2011). Functional electrical stimulation therapies after spinal cord injury. NeuroRehabilitation, 28(3), 231–248. https://doi.org/10.3233/NRE-2011-0652.

    Article  PubMed  Google Scholar 

  • Gilman, S., & Arbor, A. (1983). Handbook of physiology. Section 1: The nervous system, vol II. Motor control, parts 1 and 2. Section editors: John M. Brookhart and Vernon B. Mountcastle volume editor: Vernon B. Brooks Bethesda, MD, American Physiological Society, 1981 1480 pp, illustrated. Annals of Neurology, 13(1), 111–111. https://doi.org/10.1002/ana.410130130.

    Article  Google Scholar 

  • Gorgey, A. S., Black, C. D., Elder, C. P., & Dudley, G. A. (2009). Effects of electrical stimulation parameters on fatigue in skeletal muscle. Journal of Orthopaedic and Sports Physical Therapy, 39(9), 684–692. https://doi.org/10.2519/jospt.2009.3045.

    Article  PubMed  Google Scholar 

  • Gorgey, A. S., & Dudley, G. A. (2008). The role of pulse duration and stimulation duration in maximizing the normalized torque during neuromuscular electrical stimulation. Journal of Orthopaedic and Sports Physical Therapy, 38(8), 508–516. https://doi.org/10.2519/jospt.2008.2734.

    Article  PubMed  Google Scholar 

  • Gorgey, A. S., Graham, Z. A., Bauman, W. A., Cardozo, C., & Gater, D. R. (2017). Abundance in proteins expressed after functional electrical stimulation cycling or arm cycling ergometry training in persons with chronic spinal cord injury. Journal of Spinal Cord Medicine, 40(4), 439–448. https://doi.org/10.1080/10790268.2016.1229397.

    Article  PubMed  Google Scholar 

  • Gorgey, A. S., & Lawrence, J. (2016). Acute responses of functional electrical stimulation cycling on the ventilation-to-CO2 production ratio and substrate utilization after spinal cord injury. PM R, 8(3), 225–234. https://doi.org/10.1016/j.pmrj.2015.10.006.

    Article  PubMed  Google Scholar 

  • Griffin, L., Decker, M. J., Hwang, J. Y., Wang, B., Kitchen, K., Ding, Z., et al. (2009). Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. Journal of Electromyography and Kinesiology, 19(4), 614–622. https://doi.org/10.1016/j.jelekin.2008.03.002.

    Article  CAS  PubMed  Google Scholar 

  • Griffiths, I. R., & Miller, R. (1974). Vascular permeability to protein and vasogenic oedema in experimental concussive injuries to the canine spinal cord. Journal of the Neurological Sciences, 22(3), 291–304.

    CAS  PubMed  Google Scholar 

  • Grill, W. M., Jr., & Mortimer, J. T. (1996). The effect of stimulus pulse duration on selectivity of neural stimulation. IEEE Transactions on Biomedical Engineering, 43(2), 161–166. https://doi.org/10.1109/10.481985.

    Article  PubMed  Google Scholar 

  • Grillner, S., & Wallen, P. (1985). Central pattern generators for locomotion, with special reference to vertebrates. Annual Review of Neuroscience, 8, 233–261. https://doi.org/10.1146/annurev.ne.08.030185.001313.

    Article  CAS  PubMed  Google Scholar 

  • Guertin, P. A. (2012). Central pattern generator for locomotion: Anatomical, physiological, and pathophysiological considerations. Frontiers in Neurology, 3, 183. https://doi.org/10.3389/fneur.2012.00183.

    Article  PubMed  Google Scholar 

  • Hamid, S., & Hayek, R. (2008). Role of electrical stimulation for rehabilitation and regeneration after spinal cord injury: An overview. European Spine Journal, 17(9), 1256–1269. https://doi.org/10.1007/s00586-008-0729-3.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hansen, C. N., Faw, T. D., White, S., Buford, J. A., Grau, J. W., & Basso, D. M. (2016). Sparing of descending axons rescues interneuron plasticity in the lumbar cord to allow adaptive learning after thoracic spinal cord injury. Frontiers in Neural Circuits. https://doi.org/10.3389/fncir.2016.00011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hebb, D. (1949). The organization οf behavior. New York: Wiley.

    Google Scholar 

  • Ho, C. H., Triolo, R. J., Elias, A. L., Kilgore, K. L., DiMarco, A. F., Bogie, K., et al. (2014). Functional Electrical Stimulation and Spinal Cord Injury. Physical Medicine and Rehabilitation Clinics of North America,25 (3), 631–654. https://doi.org/10.1016/j.pmr.2014.05.001.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibitoye, M. O., Hamzaid, N. A., Hasnan, N., Abdul Wahab, A. K., & Davis, G. M. (2016). Strategies for rapid muscle fatigue reduction during FES exercise in individuals with spinal cord injury: A systematic review. PLoS ONE, 11(2), e0149024. https://doi.org/10.1371/journal.pone.0149024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh, S., Ohta, T., Sekino, Y., Yukawa, Y., & Shinomiya, K. (2008). Treatment of distal radius fractures with a wrist-bridging external fixation: The value of alternating electric current stimulation. Journal of Hand Surgery, 33(5), 605–608. https://doi.org/10.1177/1753193408092253.

    Article  CAS  PubMed  Google Scholar 

  • Kapadia, N., Masani, K., Catharine Craven, B., Giangregorio, L. M., Hitzig, S. L., Richards, K., et al. (2014a). A randomized trial of functional electrical stimulation for walking in incomplete spinal cord injury: Effects on walking competency. Journal of Spinal Cord Medicine, 37(5), 511–524. https://doi.org/10.1179/2045772314Y.0000000263.

    Article  PubMed  Google Scholar 

  • Kapadia, N. M., Bagher, S., & Popovic, M. R. (2014b). Influence of different rehabilitation therapy models on patient outcomes: Hand function therapy in individuals with incomplete SCI. Journal of Spinal Cord Medicine, 37(6), 734–743. https://doi.org/10.1179/2045772314Y.0000000203.

    Article  PubMed  Google Scholar 

  • Kebaetse, M. B., Turner, A. E., & Binder-Macleod, S. A. (2002). Effects of stimulation frequencies and patterns on performance of repetitive, nonisometric tasks. Journal of Applied Physiology, 92(1), 109–116. https://doi.org/10.1152/jappl.2002.92.1.109.

    Article  PubMed  Google Scholar 

  • Kilgore, K. L., Hoyen, H. A., Bryden, A. M., Hart, R. L., Keith, M. W., & Peckham, P. H. (2008). An implanted upper-extremity neuroprosthesis using myoelectric control. Journal of Hand Surgery-American Volume, 33a(4), 539–550. https://doi.org/10.1016/j.jhsa.2008.01.007.

    Article  Google Scholar 

  • Kjaer, M., Perko, G., Secher, N. H., Boushel, R., Beyer, N., Pollack, S., et al. (1994). Cardiovascular and ventilatory responses to electrically induced cycling with complete epidural anaesthesia in humans. Acta Physiologica Scandinavica, 151(2), 199–207. https://doi.org/10.1111/j.1748-1716.1994.tb09738.x.

    Article  CAS  PubMed  Google Scholar 

  • Kobetic, R., To, C. S., Schnellenberger, J. R., Audu, M. L., Bulea, T. C., Gaudio, R., et al. (2009). Development of hybrid orthosis for standing, walking, and stair climbing after spinal cord injury. Journal of Rehabilitation Research and Development, 46(3), 447–462.

    PubMed  Google Scholar 

  • Koyuncu, E., Nakipoglu-Yuzer, G. F., Dogan, A., & Ozgirgin, N. (2010). The effectiveness of functional electrical stimulation for the treatment of shoulder subluxation and shoulder pain in hemiplegic patients: A randomized controlled trial. Disability and Rehabilitation, 32(7), 560–566. https://doi.org/10.3109/09638280903183811.

    Article  PubMed  Google Scholar 

  • Kralj, A. R., & Bajd, T. (1989). Functional electrical stimulation: Standing and walking after spinal cord injury. Boca Raton: CRC Press.

    Google Scholar 

  • Lee, H. U., Blasiak, A., Agrawal, D. R., Loong, D. T. B., Thakor, N. V., All, A. H., et al. (2017). Subcellular electrical stimulation of neurons enhances the myelination of axons by oligodendrocytes. PLoS ONE, 12(7), e0179642. https://doi.org/10.1371/journal.pone.0179642.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loong, D. B., Chua, S. M., Prasad, A., Kakkos, I., Jiang, W. X., Yue, M., et al. (2018). Neuroprotective assessment of prolonged local hypothermia post contusive spinal cord injury in rodent model. Spine Journal, 18(3), 507–514. https://doi.org/10.1016/j.spinee.2017.10.066.

    Article  Google Scholar 

  • Lynch, C. L., & Popovic, M. R. (2008). Functional electrical stimulation. IEEE Control Systems Magazine, 28(2), 40–50.

    Google Scholar 

  • Maffiuletti, N. A., Pensini, M., & Martin, A. (2002). Activation of human plantar flexor muscles increases after electromyostimulation training. Journal of Applied Physiology, 92(4), 1383–1392. https://doi.org/10.1152/japplphysiol.00884.2001.

    Article  PubMed  Google Scholar 

  • Mangold, S., Keller, T., Curt, A., & Dietz, V. (2005). Transcutaneous functional electrical stimulation for grasping in subjects with cervical spinal cord injury. Spinal Cord, 43(1), 1–13. https://doi.org/10.1038/sj.sc.3101644.

    Article  CAS  PubMed  Google Scholar 

  • Marder, E., & Bucher, D. (2001). Central pattern generators and the control of rhythmic movements. Current Biology, 11(23), R986–996.

    CAS  PubMed  Google Scholar 

  • Martin, R., Sadowsky, C., Obst, K., Meyer, B., & McDonald, J. (2012). Functional electrical stimulation in spinal cord injury: From theory to practice. Topics in Spinal Cord Injury Rehabilitation, 18(1), 28–33.

    PubMed  Google Scholar 

  • Maybhate, A., Hu, C., Bazley, F. A., Yu, Q. L., Thakor, N. V., Kerr, C. L., et al. (2012). Potential long-term benefits of acute hypothermia after spinal cord injury: Assessments with somatosensory-evoked potentials. Critical Care Medicine, 40(2), 573–579. https://doi.org/10.1097/CCM.0b013e318232d97e.

    Article  PubMed  PubMed Central  Google Scholar 

  • McCoin, J. L., Bhadra, N., & Gustafson, K. J. (2013). Electrical stimulation of sacral dermatomes can suppress aberrant urethral reflexes in felines with chronic spinal cord injury. Neurourology and Urodynamics, 32(1), 92–97.

    PubMed  Google Scholar 

  • Med, C. S. C. (2008). Early acute management in adults with spinal cord injury: A clinical practice guideline for health-care professionals. Journal of Spinal Cord Medicine, 31(4), 403–479.

    Google Scholar 

  • Menendez, H., Ferrero, C., Martin-Hernandez, J., Figueroa, A., Marin, P. J., & Herrero, A. J. (2016). Acute effects of simultaneous electromyostimulation and vibration on leg blood flow in spinal cord injury. Spinal Cord, 54(5), 383–389. https://doi.org/10.1038/sc.2015.181.

    Article  CAS  PubMed  Google Scholar 

  • Mesin, L., Merlo, E., Merletti, R., & Orizio, C. (2010). Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle. Journal of Electromyography and Kinesiology, 20(4), 580–589. https://doi.org/10.1016/j.jelekin.2009.11.008.

    Article  CAS  PubMed  Google Scholar 

  • Mir, H., Al-Nashash, H., Kerr, D., Thakor, N., & All, A. (2010). Histogram based quantification of spinal cord injury level using somatosensory evoked potentials. In Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Embc),, (pp. 4942–4945). https://doi.org/10.1109/Iembs.2010.5627238.

  • Mir, H., Al-Nashash, H., Kortelainen, J., & All, A. (2018). Novel Modeling of somatosensory evoked potentials for the assessment of spinal cord injury. IEEE Transactions on Biomedical Engineering, 65(3), 511–520. https://doi.org/10.1109/Tbme.2017.2700498.

    Article  PubMed  Google Scholar 

  • Moe, J. H., & Post, H. W. (1962). Functional electrical stimulation for ambulation in hemiplegia. Journal-Lancet, 82(7), 285–290.

    CAS  PubMed  Google Scholar 

  • Mohr, T., Andersen, J. L., Biering-Sorensen, F., Galbo, H., Bangsbo, J., Wagner, A., et al. (1997). Long-term adaptation to electrically induced cycle training in severe spinal cord injured individuals. Spinal Cord, 35(1), 1–16.

    CAS  PubMed  Google Scholar 

  • Moritz, C. T., Perlmutter, S. I., & Fetz, E. E. (2008). Direct control of paralysed muscles by cortical neurons. Nature, 456(7222), 639–642. https://doi.org/10.1038/nature07418.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moxon, K. A., Oliviero, A., Aguilar, J., & Foffani, G. (2014). Cortical reorganization after spinal cord injury: Always for good? Neuroscience, 283, 78–94.

    CAS  PubMed  PubMed Central  Google Scholar 

  • National Cancer Institute. (n.d.). NCI dictionary of cancer terms. https://www.cancer.gov/publications/dictionaries/cancer-terms/def/nmes.

  • Center, N. S. C. I. S. (2019). Facts and figures at a glance. Birmingham, AL: University of Alabama at Birmingham.

    Google Scholar 

  • NINDS. (2013). Spinal cord injury: Hope through research. Bethesda: NIH Publication.

    Google Scholar 

  • Norenberg, M. D., Smith, J., & Marcillo, A. (2004). The pathology of human spinal cord injury: Defining the problems. New Rochelle: Mary Ann Liebert, Inc.

    Google Scholar 

  • Nuwer, M. R. (1998). Fundamentals of evoked potentials and common clinical applications today. Electroencephalography and Clinical Neurophysiology, 106(2), 142–148. https://doi.org/10.1016/S0013-4694(97)00117-X.

    Article  CAS  PubMed  Google Scholar 

  • Ojha, R., George, J., Chandy, B. R., Tharion, G., & Devasahayam, S. R. (2015). Neuromodulation by surface electrical stimulation of peripheral nerves for reduction of detrusor overactivity in patients with spinal cord injury: A pilot study. Journal of Spinal Cord Medicine, 38(2), 207–213. https://doi.org/10.1179/2045772313Y.0000000175.

    Article  PubMed  Google Scholar 

  • Okada, S. (2016). The pathophysiological role of acute inflammation after spinal cord injury. Inflammation and Regeneration. https://doi.org/10.1186/s41232-016-0026-1.

    Article  PubMed  PubMed Central  Google Scholar 

  • Partida, E., Mironets, E., Hou, S., & Tom, V. J. (2016). Cardiovascular dysfunction following spinal cord injury. Neural Regeneration Research, 11(2), 189.

    PubMed  PubMed Central  Google Scholar 

  • Peckham, P. H., & Knutson, J. S. (2005). Functional electrical stimulation for neuromuscular applications. Annual Review of Biomedical Engineering, 7, 327–360. https://doi.org/10.1146/annurev.bioeng.6.040803.140103.

    Article  CAS  PubMed  Google Scholar 

  • Petrie, M., Suneja, M., & Shields, R. K. (2015). Low-frequency stimulation regulates metabolic gene expression in paralyzed muscle. Journal of Applied Physiology, 118(6), 723–731. https://doi.org/10.1152/japplphysiol.00628.2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasad, A., Teh, D. B. L., Blasiak, A., Chai, C., Wu, Y., Gharibani, P. M., et al. (2017). Static magnetic field stimulation enhances oligodendrocyte differentiation and secretion of neurotrophic factors. Scientific Reports, 7(1), 6743. https://doi.org/10.1038/s41598-017-06331-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price, C. I., & Pandyan, A. D. (2000). Electrical stimulation for preventing and treating post-stroke shoulder pain. Cochrane Database Systematic Reviews. https://doi.org/10.1002/14651858.CD001698.

    Article  Google Scholar 

  • Ragnarsson, K. T. (2008). Functional electrical stimulation after spinal cord injury: Current use, therapeutic effects and future directions. Spinal Cord, 46(4), 255–274. https://doi.org/10.1038/sj.sc.3102091.

    Article  CAS  PubMed  Google Scholar 

  • Ralston, K. E., Harvey, L. A., Batty, J., Lee, B. B., Ben, M., Cusmiani, R., et al. (2013). Functional electrical stimulation cycling has no clear effect on urine output, lower limb swelling, and spasticity in people with spinal cord injury: A randomised cross-over trial. Journal of Physiotherapy, 59(4), 237–243.

    PubMed  Google Scholar 

  • Righetti, L., Buchli, J., & Ijspeert, A. J. (2006). Dynamic hebbian learning in adaptive frequency oscillators. Physica D: Nonlinear Phenomena, 216(2), 269–281.

    CAS  Google Scholar 

  • Roberts, T. T., Leonard, G. R., & Cepela, D. J. (2017). Classifications in brief: American Spinal Injury Association (ASIA) Impairment Scale. Clinical Orthopaedics and Related Research, 475(5), 1499–1504. https://doi.org/10.1007/s11999-016-5133-4.

    Article  PubMed  Google Scholar 

  • Robinson, A. J. (2008). Clinical electrophysiology: Electrotherapy and electrophysiologic testing. Philadelphia: Lippincott Williams & Wilkins.

    Google Scholar 

  • Rossignol, S. (2000). Locomotion and its recovery after spinal injury. Current Opinion in Neurobiology, 10(6), 708–716.

    CAS  PubMed  Google Scholar 

  • Sabut, S. K., Sikdar, C., Kumar, R., & Mahadevappa, M. (2011). Functional electrical stimulation of dorsiflexor muscle: Effects on dorsiflexor strength, plantarflexor spasticity, and motor recovery in stroke patients. NeuroRehabilitation, 29(4), 393–400. https://doi.org/10.3233/NRE-2011-0717.

    Article  PubMed  Google Scholar 

  • Sahin, N., Ugurlu, H., & Albayrak, I. (2012). The efficacy of electrical stimulation in reducing the post-stroke spasticity: A randomized controlled study. Disability and Rehabilitation, 34(2), 151–156. https://doi.org/10.3109/09638288.2011.593679.

    Article  PubMed  Google Scholar 

  • Salameh, A., Al Mohajer, M., & Daroucihe, R. O. (2015). Prevention of urinary tract infections in patients with spinal cord injury. CMAJ, 187(11), 807–811.

    PubMed  PubMed Central  Google Scholar 

  • Sieck, G. C., & Mantilla, C. B. (2004). Influence of sex hormones on the neuromuscular junction. In Advances in molecular and cell biology (Vol. 34, pp. 183–194). Amsterdam: Elsevier.

  • Sluka, K. A., & Walsh, D. (2003). Transcutaneous electrical nerve stimulation: Basic science mechanisms and clinical effectiveness. Journal of Pain, 4(3), 109–121.

    PubMed  Google Scholar 

  • Stein, R. B., Everaert, D. G., Thompson, A. K., Chong, S. L., Whittaker, M., Robertson, J., et al. (2010). Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabilitation and Neural Repair, 24(2), 152–167. https://doi.org/10.1177/1545968309347681.

    Article  PubMed  Google Scholar 

  • Szecsi, J., Fornusek, C., Krause, P., & Straube, A. (2007). Low-frequency rectangular pulse is superior to middle frequency alternating current stimulation in cycling of people with spinal cord injury. Archives of Physical Medicine and Rehabilitation, 88(3), 338–345.

    PubMed  Google Scholar 

  • Tator, C. H., & Koyanagi, I. (1997). Vascular mechanisms in the pathophysiology of human spinal cord injury. Journal of Neurosurgery, 86(3), 483–492. https://doi.org/10.3171/jns.1997.86.3.0483.

    Article  CAS  PubMed  Google Scholar 

  • Thijssen, D. H., Ellenkamp, R., Smits, P., & Hopman, M. T. (2006). Rapid vascular adaptations to training and detraining in persons with spinal cord injury. Archives of Physical Medicine and Rehabilitation, 87(4), 474–481. https://doi.org/10.1016/j.apmr.2005.11.005.

    Article  PubMed  Google Scholar 

  • Thorsen, R., Dalla Costa, D., Chiaramonte, S., Binda, L., Beghi, E., Redaelli, T., et al. (2013). A noninvasive neuroprosthesis augments hand grasp force in individuals with cervical spinal cord injury: The functional and therapeutic effects. Scientific World Journal, 2013, 836959. https://doi.org/10.1155/2013/836959.

    Article  PubMed  Google Scholar 

  • Thrasher, A., Graham, G. M., & Popovic, M. R. (2005). Reducing muscle fatigue due to functional electrical stimulation using random modulation of stimulation parameters. Artificial Organs, 29(6), 453–458.

    PubMed  Google Scholar 

  • Van Duijnhoven, N. T., Janssen, T. W., Green, D. J., Minson, C. T., Hopman, M. T., & Thijssen, D. H. (2009). Effect of functional electrostimulation on impaired skin vasodilator responses to local heating in spinal cord injury. Journal of Applied Physiology, 106(4), 1065–1071. https://doi.org/10.1152/japplphysiol.91611.2008.

    Article  PubMed  Google Scholar 

  • Vipin, A., Thow, X. Y., Mir, H., Kortelainen, J., Manivannan, J., Al-Nashash, H., et al. (2016). Natural progression of spinal cord transection injury and reorganization of neural pathways. Journal of Neurotrauma, 33(24), 2191–2201. https://doi.org/10.1089/neu.2015.4383.

    Article  PubMed  Google Scholar 

  • Wahls, T. L., Reese, D., Kaplan, D., & Darling, W. G. (2010). Rehabilitation with neuromuscular electrical stimulation leads to functional gains in ambulation in patients with secondary progressive and primary progressive multiple sclerosis: A case series report. Journal of Alternative and Complementary Medicine, 16(12), 1343–1349. https://doi.org/10.1089/acm.2010.0080.

    Article  PubMed  Google Scholar 

  • Wan, J. J., Qin, Z., Wang, P. Y., Sun, Y., & Liu, X. (2017). Muscle fatigue: General understanding and treatment. Experimental & Molecular Medicine, 49(10), e384. https://doi.org/10.1038/emm.2017.194.

    Article  CAS  Google Scholar 

  • Wheeler, G. D., Andrews, B., Lederer, R., Davoodi, R., Natho, K., Weiss, C., et al. (2002). Functional electric stimulation-assisted rowing: Increasing cardiovascular fitness through functional electric stimulation rowing training in persons with spinal cord injury. Archives of Physical Medicine and Rehabilitation, 83(8), 1093–1099.

    PubMed  Google Scholar 

  • Wilbanks, S. R., Rogers, R., Pool, S., & Bickel, C. S. (2016). Effects of functional electrical stimulation assisted rowing on aerobic fitness and shoulder pain in manual wheelchair users with spinal cord injury. Journal of Spinal Cord Medicine, 39(6), 645–654. https://doi.org/10.1179/2045772315Y.0000000052.

    Article  PubMed  Google Scholar 

  • Yarar-Fisher, C., Bickel, C. S., Windham, S. T., McLain, A. B., & Bamman, M. M. (2013). Skeletal muscle signaling associated with impaired glucose tolerance in spinal cord-injured men and the effects of contractile activity. Journal of Applied Physiology, 115(5), 756–764. https://doi.org/10.1152/japplphysiol.00122.2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yasar, E., Yilmaz, B., Goktepe, S., & Kesikburun, S. (2015). The effect of functional electrical stimulation cycling on late functional improvement in patients with chronic incomplete spinal cord injury. Spinal Cord, 53(12), 866–869. https://doi.org/10.1038/sc.2015.19.

    Article  CAS  PubMed  Google Scholar 

  • Young, S., Hampton, S., & Tadej, M. (2011). Study to evaluate the effect of low-intensity pulsed electrical currents on levels of oedema in chronic non-healing wounds. Journal of Wound Care, 20(8), 368. https://doi.org/10.12968/jowc.2011.20.8.368.

    Article  CAS  PubMed  Google Scholar 

  • Young, W. (2015). Electrical stimulation and motor recovery. Cell Transplantation, 24(3), 429–446. https://doi.org/10.3727/096368915X686904.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Johns Hopkins Welch Medical Library Informationist Mr. Robert Wright, MLS for providing his expertise and assistance with the PubMed database search. We would also like to acknowledge the contributions of Ms. Alisa Brown, Mr. Michael Pozin, Ms. Nausheen Tickoo, and Ms. Shichen Zhang for their efforts of preliminary literature search and data mining. The illustrations of this article were created with Biorender.com following an academic licensing agreement.

Funding

The study received no external funding.

Author information

Authors and Affiliations

Authors

Contributions

AA, SL, HX and YZ contributed to the conception and design. SL, HX and YZ performed literature search and data analysis. SL and HX drafted the paper. XL provided critical revision of the work. AA supervised and reviewed this study.

Corresponding authors

Correspondence to Xiaogang Liu or Angelo H. All.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, S., Xu, H., Zuo, Y. et al. A Review of Functional Electrical Stimulation Treatment in Spinal Cord Injury. Neuromol Med 22, 447–463 (2020). https://doi.org/10.1007/s12017-019-08589-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12017-019-08589-9

Keywords

Navigation