Topical electrostimulation for correction of respiratory disorders in spinal cord injury: A review

Abstract

BACKGROUND: A spinal cord injury can lead to paralysis of the respiratory muscles, resulting in a significant reduction in breathing ability. People with a spinal cord injury face an increased risk of developing various respiratory complications. To date, existing effective technologies positively affect the long-term recovery of respiratory function and create conditions for neuroplasticity in the injured spinal cord. The high relevance and lack of systematization of these techniques in the world literature served as the basis for describing a topical approach in electrostimulation for the correction of respiratory disorders in patients with traumatic spinal cord injuries.

AIM: To formulate an algorithm for topical electrostimulation of the spinal cord and respiratory muscles to correct respiratory dysfunction in patients with spinal cord injury based on the latest scientific literature.

MATERIALS AND METHODS: This article presents the results of the analysis of peer-reviewed articles that investigated the effects of various electrostimulation techniques on respiratory function in patients with spinal cord injury. Searches were performed on ScienceDirect, Google Scholar, and PubMed for the period from 2000 to 2022.

RESULTS: A spinal cord and muscle electrostimulation algorithm was formulated to personalize the treatment approach for patients with spinal cord injury depending on the level and period of traumatic spinal cord injury.

CONCLUSIONS: Electrostimulation techniques were found to be effective in the treatment of spinal cord injuries, particularly for the correction of respiratory disorders. The choice of the appropriate neurostimulation technique depends on the severity, injury level, and period of injury. Noninvasive techniques, such as FES and TSSM, can be used from the acute period to the chronic period, whereas invasive techniques, such as epidural stimulation and respiratory pacemaker placement, are appropriate in the chronic period. Despite the positive results of these techniques, further research is needed to develop effective treatment plans and improve their effectiveness and long-term outcomes.

Keywords

spinal cord injury / mechanical ventilation / respiratory muscle palsy / neuroprosthesis / neuroplasticity / neuromodulation / electrical stimulation / rhythm generator / rehabilitation

References

[1] DiMarco AF. Neural prostheses in the respiratory system. J Rehabil Res Dev. 2001;38(6):601–607.

[2] Dimarco A.F. Neural prostheses in the respiratory system // J. Rehabil. Res. Dev. 2001. Vol. 38. No. 6. P. 601–607.

[3] Sezer N, Akkuş S, Uğurlu FG. Chronic complications of spinal cord injury. World J Orthop. 2015;6(1):24–33. DOI: 10.5312/wjo.v6.i1.24

[4] Sezer N., Akkuş S., Uğurlu F.G. Chronic complications of spinal cord injury // World J. Orthop. 2015. Vol. 6. No. 1. P. 24–33. DOI: 10.5312/wjo.v6.i1.24

[5] Tester NJ, Fuller DD, Fromm JS, et al. Long-term facilitation of ventilation in humans with chronic spinal cord injury. Am J Respir Crit Care Med. 2014;189(1):57–65. DOI: 10.1164/rccm.201305-0848oc

[6] Tester N.J., Fuller D.D., Fromm J.S., et al. Long-term facilitation of ventilation in humans with chronic spinal cord injury // Am. J. Respir. Crit. Care Med. 2014. Vol. 189. No. 1. P. 57–65. DOI: 10.1164/rccm.201305-0848oc

[7] Berlly M, Shem K. Respiratory management during the first five days after spinal cord injury. J Spinal Cord Med. 2007;30(4):309–318. DOI: 10.1080/10790268.2007.11753946

[8] Berlly M., Shem K. Respiratory management during the first five days after spinal cord injury // J. Spinal Cord. Medicine. 2007. Vol. 30. No. 4. P. 309–318. DOI: 10.1080/10790268.2007.11753946

[9] Jarosz R, Littlepage MM, Creasey G, et al. Functional electrical stimulation in spinal cord injury respiratory care. Top Spinal Cord Inj Rehabil. 2012;18(4):315–321. DOI: 10.1310/sci1804-315

[10] Jarosz R., Littlepage M.M., Creasey G., et al. Functional electrical stimulation in spinal cord injury respiratory care // Top. Spinal Cord Inj. Rehabil. 2012. Vol. 18. No. 4. P. 315–321. DOI: 10.1310/sci1804-315

[11] Adler D, Gonzalez-Bermejo J, Duguet A, et al. Diaphragm pacing restores olfaction in tetraplegia. Eur Respir J. 2008;34(2):365–370. DOI: 10.1183/09031936.00177708

[12] Adler D., Gonzalez-Bermejo J., Duguet A., et al. Diaphragm pacing restores olfaction in tetraplegia // Eur. Respir. J. 2008. Vol. 34. No. 2. P. 365–370. DOI: 10.1183/09031936.00177708

[13] Hachmann JT, Grahn PJ, Calvert JS, et al. Electrical neuromodulation of the respiratory system after spinal cord injury. Mayo Clin Proc. 2017;92(9):1401–1414. DOI: 10.1016/j.mayocp.2017.04.011

[14] Hachmann J.T., Grahn P.J., Calvert J.S., et al. Electrical neuromodulation of the respiratory system after spinal cord injury // Mayo Clin. Proceed. 2017. Vol. 92. No. 9. P. 1401–1414. DOI: 10.1016/j.mayocp.2017.04.011

[15] Gray’s anatomy 41st edition: the anatomical basis of clinical practice. Ed. by S. Standring. Elsevier Science; 2015.

[16] Gray’s anatomy 41st edition: the anatomical basis of clinical practice / ed. by S. Standring. Elsevier Science, 2015.

[17] Terson de Paleville D, Lorenz D. Compensatory muscle activation during forced respiratory tasks in individuals with chronic spinal cord injury. Respir Physiol Neurobiol. 2015;217:54–62. DOI: 10.1016/j.resp.2015.07.001

[18] Terson de Paleville D., Lorenz D. Compensatory muscle activation during forced respiratory tasks in individuals with chronic spinal cord injury // Respir. Physiol. Neurobiol. 2015. Vol. 217. P. 54–62. DOI: 10.1016/j.resp.2015.07.001

[19] Smith JC, Abdala AP, Koizumi H, et al. Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol. 2007;98(6):3370–3387. DOI: 10.1152/jn.00985.2007

[20] Smith J.C., Abdala A.P., Koizumi H., et al. Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms // J. Neurophysiol. 2007. Vol. 98. No. 6. P. 3370–3387. DOI: 10.1152/jn.00985.2007

[21] Paton JF, Abdala AP, Koizumi H, et al. Respiratory rhythm generation during gasping depends on persistent sodium current. Nat Neurosci. 2006;9(3):311–333. DOI: 10.1038/nn1650

[22] Paton J.F.R., Abdala A.P., Koizumi H., et al. Respiratory rhythm generation during gasping depends on persistent sodium current // Nat. Neurosci. 2006. Vol. 9. No. 3. P. 311–313. DOI: 10.1038/nn1650

[23] De Troyer A, Kirkwood PA, Wilson TA. Respiratory action of the intercostal muscles. Physiol Rev. 2005;85(2):717–756. DOI: 10.1152/physrev.00007.2004

[24] De Troyer A., Kirkwood P.A., Wilson T.A. Respiratory action of the intercostal muscles // Physiol. Rev. 2005. Vol. 85. No. 2. P. 717–756. DOI: 10.1152/physrev.00007.2004

[25] De Troyer A, Gorman RB, Gandevia SC. Distribution of inspiratory drive to the external intercostal muscles in humans. J Physiol. 2003;546:943–954. DOI: 10.1113/jphysiol.2002.028696

[26] De Troyer A., Gorman R.B., Gandevia S.C. Distribution of inspiratory drive to the external intercostal muscle in humans // J. Physiol. 2003. Vol. 546. No. 3. P. 943–954. DOI: 10.1113/jphysiol.2002.028696

[27] Gandevia SC, Hudson AL, Gorman RB, et al. Spatial distribution of inspiratory drive to the parasternal intercostal muscles in humans. J Physiol. 2006;573:263–275. DOI: 10.1113/jphysiol.2005.101915

[28] Gandevia S.C., Hudson A.L., Gorman R.B., et al. Spatial distribution of inspiratory drive to the parasternal intercostal muscles in humans // J. Physiol. 2006. Vol. 573. No. 1. P. 263–275. DOI: 10.1113/jphysiol.2005.101915

[29] Zaki Ghali MG, Britz G, Lee KZ. Pre-phrenic interneurons: Characterization and role in phrenic pattern formation and respiratory recovery following spinal cord injury. Respir Physiol Neurobiol. 2019;265:24–31. DOI: 10.1016/j.resp.2018.09.005

[30] Zaki Ghali M.G., Britz G., Lee K.Z. Pre-phrenic interneurons: Characterization and role in phrenic pattern formation and respiratory recovery following spinal cord injury // Respir. Physiol. Neurobiol. 2019. Vol. 265. P. 24–31. DOI: 10.1016/j.resp.2018.09.005

[31] Caughey EJ, Borotkanics RJ, Gollee H, et al. Abdominal functional electrical stimulation to improve respiratory function after spinal cord injury: a systematic review and meta-analysis. Spinal Cord. 2016;54(9):628–639. DOI: 10.1038/sc.2016.31

[32] McCaughey E.J., Borotkanics R.J., Gollee H., et al. Abdominal functional electrical stimulation to improve respiratory function after spinal cord injury: a systematic review and meta-analysis // Spinal Cord. 2016. Vol. 54. No. 9. P. 628–639. DOI: 10.1038/sc.2016.31

[33] Gad P, Kreydin E, Zhong H, et al. Enabling respiratory control after severe chronic tetraplegia: an exploratory case study. J Neurophysiol. 2020;124(3):774–780. DOI: 10.1152/jn.00320.2020

[34] Gad P., Kreydin E., Zhong H., et al. Enabling respiratory control after severe chronic tetraplegia: an exploratory case study // J. Neurophysiol. 2020. Vol. 124. No. 3. P. 774–780. DOI: 10.1152/jn.00320.2020

[35] Minyaeva AV, Moiseev SA, Pukhov AM, et al. Response of external inspiration to the movements induced by transcutaneous spinal cord stimulation. Hum Physiol. 2017;43:524–531. DOI: 10.1134/s0362119717050115

[36] Minyaeva A.V., Moiseev S.A., Pukhov A.M, et al. Response of external inspiration to the movements induced by transcutaneous spinal cord stimulation // Hum. Physiol. 2017. Vol. 43. No. 5. P. 524–531. DOI: 10.1134/s0362119717050115

[37] Keller A, Singh G, Sommerfeld JH, et al. Noninvasive spinal stimulation safely enables upright posture in children with spinal cord injury. Nat. Commun. 2021;12(1). DOI: 10.1038/s41467-021-26026-z

[38] Keller A., Singh G., Sommerfeld J.H., et al. Noninvasive spinal stimulation safely enables upright posture in children with spinal cord injury // Nat. Commun. 2021. Vol. 12. No. 1. DOI: 10.1038/s41467-021-26026-z

[39] Joffe JR. The effect of functional electrical stimulation on abdominal muscle strength and gross motor function in children with cerebral palsy a randomised control trial [dissertation]. Cape Town: University of Cape Town; 2014.

[40] Joffe J.R. The effect of functional electrical stimulation on abdominal muscle strength and gross motor function in children with cerebral palsy a randomised control trial: dissertation. Cape Town: University of Cape Town; 2014.

[41] Averybiomedical.com [Internet] Avery Biomedical devices – leader in diaphragm pacemakers [cited 2022 Dec 20]. Available from: http://www.averybiomedical.com

[42] Averybiomedical.com [Internet] Avery Biomedical devices – leader in diaphragm pacemakers [дата обращения 20.12.2022]. Доступ по ссылке: http://www.averybiomedical.com

[43] Dalal K, DiMarco AF. Diaphragmatic pacing in spinal cord injury. Phys Med Rehabil Clin N Am. 2014;25(3):619–629. DOI: 10.1016/j.pmr.2014.04.004

[44] Dalal K., DiMarco A.F. Diaphragmatic pacing in spinal cord injury // Physical. Med. Rehabil. Clin. N. Am. 2014. Vol. 25. No. 3. P. 619–629. DOI: 10.1016/j.pmr.2014.04.004

[45] Posluszny JA Jr, Onders R, Kerwin AJ, et al. Multicenter review of diaphragm pacing in spinal cord injury: successful not only in weaning from ventilators but also in bridging to independent respiration. J Trauma Acute Care Surg. 2014;76(2):303–309. DOI: 10.1097/ta.0000000000000112

[46] Posluszny J.A. Jr., Onders R., Kerwin A.J., et al. Multicenter review of diaphragm pacing in spinal cord injury: successful not only in weaning from ventilators but also in bridging to independent respiration // J. Trauma Acute Care Surg. 2014. Vol. 76. No. 2. P. 303–309. DOI: 10.1097/ta.0000000000000112

[47] Bakr SM, Knight J, Johnson SK, et al. Spinal cord stimulation improves functional outcomes in children with complex regional pain syndrome: case presentation and review of the literature. Pain Pract. 2020;20(6):647–655. DOI: 10.1111/papr.12882

[48] Bakr S.M., Knight J., Johnson S.K., et al. Spinal cord stimulation improves functional outcomes in children with complex regional pain syndrome: case presentation and review of the literature // Pain Practice. 2020. Vol. 20. No. 6. P. 647–655. DOI: 10.1111/papr.12882

[49] DiMarco AF, Kowalski KE. Intercostal muscle pacing with high frequency spinal cord stimulation in dogs. Respir Physiol Neurobiol. 2010;171(3):218–24. DOI: 10.1016/j.resp.2010.03.017

[50] DiMarco A.F., Kowalski K.E. Intercostal muscle pacing with high frequency spinal cord stimulation in dogs // Respir. Physiol. Neurobiol. 2010. Vol. 171. No. 3. P. 218–224. DOI: 10.1016/j.resp.2010.03.017

[51] Adachi T, Yokoyama M, Onuki T. Experimental evaluation of the optimal tidal volume for simultaneous pacing of the diaphragm and respiratory muscles. J Artif Organs. 2004;7(1):27–29. DOI: 10.1007/s10047-003-0246-4

[52] Adachi T., Yokoyama M., Onuki T. Experimental evaluation of the optimal tidal volume for simultaneous pacing of the diaphragm and respiratory muscles // J. Artif. Organs. 2004. Vol. 7. No. 1. P. 27–29. DOI: 10.1007/s10047-003-0246-4

[53] Tator CH, Minassian K, Mushahwar VK. Spinal cord stimulation: therapeutic benefits and movement generation after spinal cord injury. Handb Clin Neurol. 2012;109:283–296. DOI: 10.1016/B978-0-444-52137-8.00018-8

[54] Tator C.H., Minassian K., Mushahwar V.K. Spinal cord stimulation: therapeutic benefits and movement generation after spinal cord injury // Handbook Clin. Neurol. 2012. Vol. 109. P. 283–296. DOI: 10.1016/B978-0-444-52137-8.00018-8

[55] 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. DOI: 10.1093/brain/awu038

[56] Angeli C.A., Edgerton V.R., Gerasimenko Y.P., et al. Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans // Brain. 2014. Vol. 137. No. 5. DOI: 10.1093/brain/awu038

[57] 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(9781):1938–1947. DOI: 10.1016/s0140-6736(11)60547-3

[58] 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. Vol. 377. No. 9781. P. 1938–1947. DOI: 10.1016/s0140-6736(11)60547-3

[59] Saywell SA, Ford TW, Meehan CF, et al. Electrophysiological and morphological characterization of propriospinal interneurons in the thoracic spinal cord. J Neurophysiol. 2011;105(2):806–826. DOI: 10.1152/jn.00738.2010

[60] Saywell S.A., Ford T.W., Meehan C.F., et al. Electrophysiological and morphological characterization of propriospinal interneurons in the thoracic spinal cord // J. Neurophysiol. 2011. Vol. 105. No. 2. P. 806–826. DOI: 10.1152/jn.00738.2010

[61] Iizuka M, Onimaru H, Izumizaki M. Distribution of respiration-related neuronal activity in the thoracic spinal cord of the neonatal rat: an optical imaging study. Neuroscience. 2016;315:217–227. DOI: 10.1016/j.neuroscience.2015.12.015

[62] Iizuka M., Onimaru H., Izumizaki M. Distribution of respiration-related neuronal activity in the thoracic spinal cord of the neonatal rat: an optical imaging study // Neuroscience. 2016. Vol. 315. P. 217–227. DOI: 10.1016/j.neuroscience.2015.12.015

[63] DiMarco AF, Kowalski KE. Activation of inspiratory muscles via spinal cord stimulation. Respir Physiol Neurobiol. 2013;189(2):438–449. DOI: 10.1016/j.resp.2013.06.001

[64] DiMarco A.F., Kowalski K.E. Activation of inspiratory muscles via spinal cord stimulation // Respir. Physiol. Neurobiol. 2013. Vol. 189. No. 2. P. 438–449. DOI: 10.1016/j.resp.2013.06.001

[65] DiMarco AF, Kowalski KE. Activation of the expiratory muscles via lower thoracic high frequency spinal cord stimulation in awake animals. Respir Physiol Neurobiol. 2020;276. DOI: 10.1016/j.resp.2019.103360

[66] DiMarco A.F., Kowalski K.E. Activation of the expiratory muscles via lower thoracic high frequency spinal cord stimulation in awake animals // Respir. Physiol. Neurobiol. 2020. Vol. 276. DOI: 10.1016/j.resp.2019.103360

[67] Toriya VG, Vissarionov SV, Kubanov RR, et al. Personalized application of electrostimulation techniques for correction and accelerated recovery of respiratory disorders in spinal cord injury. Certificate of DB registration. RU 2023621031, 2023. (In Russ.)

[68] Тория В.Г., Виссарионов С.В., Кубанов Р.Р., и др. Персонифицированное применение методик электростимуляции для коррекции и ускоренного восстановления дыхательных расстройств при травме спинного мозга: Свидетельство о регистрации базы данных № 2023621031 RU, 2023.