РЕГУЛЯЦИЯ ДЫХАНИЯ ЧЕЛОВЕКА С ПОМОЩЬЮ ЭЛЕКТРИЧЕСКОЙ СТИМУЛЯЦИИ
PDF

Ключевые слова

дыхание
стимуляция спинного мозга
электрическая стимуляция диафрагмы
чрескожная стимуляция
искусственная вентиляция лёгких
травма спинного мозга

Как цитировать

Шандыбина, Н. Д., Куропатенко, М. В., & Мошонкина, Т. Р. (2022). РЕГУЛЯЦИЯ ДЫХАНИЯ ЧЕЛОВЕКА С ПОМОЩЬЮ ЭЛЕКТРИЧЕСКОЙ СТИМУЛЯЦИИ. Российский физиологический журнал им. И. М. Сеченова, 108(11), 1410–1425. https://doi.org/10.31857/S0869813922110115

Аннотация

В обзоре рассмотрены современные методы электростимуляции, используемые для регуляции функции внешнего дыхания у человека, а именно, абдоминальная функциональная стимуляция дыхательных мышц, стимуляция диафрагмы, стимуляция диафрагмального нерва, эпидуральная и чрескожная стимуляция спинного мозга. Для каждого из методов описаны физиологические основы их применения, приведены примеры использования в клинике, в том числе, указаны параметры стимуляции и локализация электродов. Проанализирована целесообразность применения каждого из методов электростимуляции у пациентов с парезом дыхательной мускулатуры и особенности их применения в зависимости от уровня травмы спинного мозга, сохранности нервных волокон. Методу эпидуральной стимуляции спинного мозга уделено особое внимание, так как этот метод применяется в электрофизиологических исследованиях на животных моделях и дает знания о спинальных уровнях регуляции функции внешнего дыхания. В обзоре обоснован большой потенциал использования метода чрескожной электрической стимуляции спинного мозга как в фундаментальных исследованиях функции внешнего дыхания, так и в клинической практике.

https://doi.org/10.31857/S0869813922110115
PDF

Литература

Safonov VA, Tarasova NN (2010) Electrical Stimulation оf Breathing. Human Physiol 36:483–494.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration J Сlin Epidemiol 62(10):ppe1-e34. https://doi.org/10.1136/bmj.b2700

McCaughey EJ, Berry HR, McLean AN, Allan DB, Gollee H (2015) Abdominal functional electrical stimulation to assist ventilator weaning in acute tetraplegia: A cohort study. PLoS One10 (6): e0128589. https://doi.org/10.1371/journal.pone.0128589

Lim J, Gorman RB, Saboisky JP, Gandevia SC, Butler JE (2007) Optimal electrode placement for noninvasive electrical stimulation of human abdominal muscles. J Appl Physiol 102(4):1612–1617. https://doi.org/10.1152/japplphysiol.00865.2006

Butler JE, Lim J, Gorman RB, Boswell-Ruys C, Saboisky JP, Lee BB, Gandevia SC (2011) Posterolateral surface electrical stimulation of abdominal expiratory muscles to enhance cough in spinal cord injury. Neurorehabil Neural Repair 25 158–167. https://doi.org/10.1177/1545968310378509

McCaughey EJ, Butler JE, McBain RA, Boswell-Ruys CL, Hudson AL, Gandevia SC, Lee BB (2019) Abdominal functional electrical stimulation to augment respiratory function in spinal cord injury. Top Spinal Cord Inj Rehabil 25(2):105–111. https://doi.org/10.1310/sci2502-105

Duarte GL, Bethiol AL, Ratti LD, Franco G, Moreno R, Tonella RM, Falcão AL (2021) Transcutaneous electrical diaphragmatic stimulation reduces the duration of invasive mechanical ventilation in patients with cervical spinal cord injury: retrospective case series. Spinal Cord Series Cases 7(1):1–6. https://doi.org/10.1038/s41394-021-00396-4

Hsin YF, Chen SH, Yu TJ, Huang CC, Chen YH (2022) Effects of transcutaneous electrical diaphragmatic stimulation on respiratory function in patients with prolonged mechanical ventilation. Ann Thorac Med 17(1):14–20. https://doi.org/10.4103/atm.atm_158_21

Postma K, Haisma JA, Hopman MT, Bergen MP, Stam HJ, Bussmann JB (2014) Resistive inspiratory muscle training in people with spinal cord injury during inpatient rehabilitation: a randomized controlled trial. Phys Therapy 94:1709–1719. https://doi.org/10.2522/ptj.20140079

Gattinoni L, Marini JJ, Collino F, Maiolo G, Rapetti F, Tonetti T, Vasques F, Quintel M (2017) The future of mechanical ventilation: lessons from the present and the past. Crit Care 21(1):183. https://doi.org/10.1186/s13054-017-1750-x

Levy M, Mizrahi J, Susak Z (1990) Recruitment, force and fatigue characteristics of 768 quadriceps muscles of paraplegics isometrically activated by surface functional 769 electrical stimulation. J Engin 12: 150–156. https://doi.org/10.1016/0141-5425(90)90136-B

DiMarco AF (2001) Neural prostheses in the respiratory system. J Rehabil Res Develop 38:601–607.

Glenn WW, Brouillette RT, Dentz B, Fodstad H, Hunt CE, Keens TG, Marsh HM, Pande S, Piepgras DG, Vanderlinden RG (1988) Fundamental considerations in pacing of the diaphragm for chronic ventilatory insufficiency. A multi-center study. Pacing Clin Electrophysiol 11:2121–2127. https://doi.org/10.1111/j.1540-8159.1988.tb06360.x

Onders RP, Elmo M, Khansarinia S, Bowman B, Yee J, Road J, Bass B, Dunkin B, Ingvarsson PE, Oddsdóttir M (2009) Complete Worldwide Operative Experience in Laparoscopic Diaphragm Pacing: Results and Differences in Spinal Cord Injured Patients and Amyotrophic Lateral Sclerosis Patients. Surg Endoscopy 23: 1433–1440. https://doi.org/10.1007/s00464-008-0223-3

DiMarco AF (2009) Phrenic nerve stimulation in patients with spinal cord injury. Respirat Physiol Neurobiol 169(2):200–209. https://doi.org/10.1016/j.resp.2009.09.008

Romero-Ganuza FJ, Gambarrutta-Malfatti C, Diez de la Lastra-Buigues E, Marín-Ruiz MÁ, Merlo-González VE, Sánchez-Aranzueque Pantoja AM, García-Moreno FJ, Mazaira-Álvarez J (2011) Diaphragmatic pacemaker as an alternative to mechanical ventilation in patients with cervical spinal injury. Med Intensiva (Engl Edition) 35:13–21. https://doi.org/10.1016/j.medin.2010.10.003

Locke KC, Randelman ML, Hoh DJ, Zholudeva LV, Lane MA (2022) Respiratory plasticity following spinal cord injury. Neural Regen Res 17:2141–2148. https://doi.org/10.4103/1673-5374.335839

Onders RP, Elmo M, Kaplan C, Schilz R, Katirji B, Tinkoff G (2018) Long-term experience with diaphragm pacing for traumatic spinal cord injury: early implantation should be considered. Surgery 164(4):705–711. https://doi.org/10.1016/j.surg.2018.06.050

Son BC, Kim DR, Kim IS, Hong JT (2013) Phrenic nerve stimulation for diaphragm pacing in a quadriplegic patient. J Korean Neurosurg Soc 54(4):359–362. https://doi.org/10.3340/jkns.2013.54.4.359

Vázquez RG, Sedes PR, Fariña MM, Marqués AM, Velasco MEF (2013) Respiratory Management in the Patient with Spinal Cord Injury. Biomed Res Int 2013:168757. https://doi.org/10.1155/2013/168757

Verrills P, Sinclair C, Barnard A (2016) A review of spinal cord stimulation systems for chronic pain. J Pain Res 9:481. https://doi.org/10.2147/JPR.S108884

Pérez JT (2021) Spinal cord stimulation: beyond pain management. Neurología (Engl Edition). https://doi.org/10.1016/j.nrleng.2019.05.007

Stauss T, El Majdoub F, Sayed D, Surges G, Rosenberg WS, Kapural L, Bundschu R, Lalkhen A, Patel N, Gliner B, Subbaroyan J (2019) A multicenter real‐world review of 10 kH z SCS outcomes for treatment of chronic trunk and/or limb pain. Ann Clin Translat Neurol 6:496–507. https://doi.org/10.1002/acn3.720

Baranidharan G, Bretherton B, Montgomery C, Titterington J, Crowther T, Vannabouathong C, Inzana JA, Rotte A (2021) Pain Relief and Safety Outcomes with Cervical 10 kHz Spinal Cord Stimulation: Systematic Literature Review and Meta-analysis. Pain and Therapy 10:849–874. https://doi.org/10.1007/s40122-021-00269-6

Kumar K, Taylor RS, Jacques L, Eldabe S, Meglio M, Molet J, Thomson S, O’Callaghan J, Eisenberg E, Milbouw G, Buchser E (2007) Spinal cord stimulation versus conventional medical management for neuropathic pain: a multicentre randomised controlled trial in patients with failed back surgery syndrome. Pain 132:179–188. https://doi.org/10.1016/j.pain.2007.07.028

Medtronic Indications, Safety & Warnings for Spinal Cord Stimulation Medtronic (2018) Accessed April 4th, 2022.

Angeli CA, Edgerton VR, Gerasimenko YP, Harkema SJ (2014) Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans. Brain 137:1394–1409. https://doi.org/10.1093/brain/awu038

Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y, Ferreira C, Willhite A, Rejc E, Grossman RG, Edgerton VR (2011) Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 377:1938–1947. https://doi.org/10.1016/S0140-6736(11)60547-3

Hachmann JT, Yousak A, Wallner JJ, Gad PN, Edgerton VR, Gorgey AS (2021) Epidural spinal cord stimulation as an intervention for motor recovery after motor complete spinal cord injury. J Neurophysiol 126(6):1843–1859. https://doi.org/10.1152/jn.00020.2021

Gerasimenko YP, Lu DC, Modaber M, Zdunowski S, Gad P, Sayenko DG, Morikawa E, Haakana P, Ferguson AR, Roy RR, Edgerton VR (2015) Noninvasive reactivation of motor descending control after paralysis. J Neurotrauma 32:1968–1980. https://doi.org/10.1089/neu.2015.4008

Gerasimenko Y, Gorodnichev R, Puhov A, Moshonkina T, Savochin A, Selionov V, Roy RR, Lu DC, Edgerton VR (2015) Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans. J Neurophysiol 113:834–842. https://doi.org/10.1152/jn.00609.2014

Gorodnichev RM, Pivovarova EA, Pukhov A, Moiseev SA, Savokhin AA, Moshonkina TR, Shcherbakova NA, Kilimnik VA, Selionov VA, Kozlovskaia IB, Edgerton VR, Gerasimenko YP (2012) Transcutaneous electrical stimulation of the spinal cord: non-invasive tool for activation of locomotor circuitry in human. Human Physiol 38:46–56.

Megia Garcia A, Serrano-Muñoz D, Taylor J, Avendaño-Coy J, Gómez-Soriano J (2020) Transcutaneous spinal cord stimulation and motor rehabilitation in spinal cord injury: a systematic review. Neurorehabil Neural Repair 34(1):3–12. https://doi.org/10.1177/1545968319893298

Gerasimenko Y, Gorodnichev R, Puhov A, Moshonkina T, Savochin A, Selionov V, Roy RR, Lu DC, Edgerton VR (2015) Initiation and modulation of locomotor circuitry output with multisite transcutaneous electrical stimulation of the spinal cord in noninjured humans. J Neurophysiol 113(3):834–842. https://doi.org/10.1152/jn.00609.2014

Grishin AA, Bobrova EV, Reshetnikova VV, Moshonkina TR, Gerasimenko YP (2021) A system for detecting stepping cycle phases and spinal cord stimulation as a tool for controlling human locomotion. Biomed Engineer 54(5):312–316. https://doi.org/10.1007/s10527-021-10029-7

Sunshine MD, Sutor TW, Fox EJ, Fuller DD (2020) Targeted activation of spinal respiratory neural circuits. Exp Neurol 328:113256. https://doi.org/10.1016/j.expneurol.2020.113256

Lane MA, White TE, Coutts MA, Jones AL, Sandhu MS, Bloom DC, Bolser DC, Yates BJ, Fuller DD, Reier PJ (2008) Cervical prephrenic interneurons in the normal and lesioned spinal cord of the adult rat. J Compar Neurol 511(5):692–709. https://doi.org/10.1002/cne.21864

Duffin J, Hoskin RW (1987) Intracellular recordings from upper cervical inspiratory neurons in the cat. Brain Res 435: 351–354. https://doi.org/10.1016/0006-8993(87)91623-4

Lipski J, Duffin J (1986) An electrophysiological investigation of propriospinal inspiratory neurons in the upper cervical cord of the cat. Exp Brain Res 61: 625–637. https://doi.org/10.1007/BF00237589

Bellingham MC, Lipski J (1990) Respiratory interneurons in the C5 segment of the spinal cord of the cat. Brain Res 533(1):141–146. https://doi.org/10.1016/0006-8993(90)91807-S

Duffin J, Iscoe S (1996) The possible role of C5 segment inspiratory interneurons investigated by cross-correlation with phrenic motoneurons in decerebrate cats. Exp Brain Res 112(1):35–40. https://doi.org/10.1007/BF00227175

Palisses R, Persegol L, Viala D (1989) Evidence for respiratory interneurones in the C3-C5 cervical spinal cord in the decorticate rabbit. Exp Brain Res 78(3):624–632. https://doi.org/10.1007/BF00230250

DiMarco AF, Kowalski KE (2013) Spinal pathways mediating phrenic activation during high frequency spinal cord stimulation. Resp Physiol Neurobiol 186:1–6. https://doi.org/10.1016/j.resp.2012.12.003

Kowalski KE, Romaniuk JR, Kirkwood PA, DiMarco AF (2019) Inspiratory muscle activation via ventral lower thoracic high-frequency spinal cord stimulation. J Appl Physiol (1985) 126: 977–983. https://doi.org/10.1152/japplphysiol.01054.2018

DiMarco AF, Kowalski KE (2013) Activation of inspiratory muscles via spinal cord stimulation. Respir Physiol Neurobiol 189: 438–449. https://doi.org/10.1016/j.resp.2013.06.001

DiMarco AF, Romaniuk JR, Kowalski KE, Supinski G (1999) Pattern of expiratory muscle activation during lower thoracic spinal cord stimulation. J Appl Physiol 86: 1881–1889. https://doi.org/10.1152/jappl.1999.86.6.1881

DiMarco AF, Kowalski KE (2008) Effects of chronic electrical stimulation on paralyzed expiratory muscles. J Appl Physiol 104(6):1634–1640. https://doi.org/10.1152/japplphysiol.01321.2007

Kowalski KE, Romaniuk JR, Kowalski T, DiMarco AF (2017) Effects of expiratory muscle activation via high-frequency spinal cord stimulation. J Appl Physiol 123(6):1525–1531. https://doi.org/10.1152/japplphysiol.00402.2017

Kastner A, Gauthier P (2008) Are rodents an appropriate pre-clinical model for treating spinal cord injury? Examples from the respiratory system. Exp Neurol 213(2):249–256. https://doi.org/10.1016/j.expneurol.2008.07.008

Mercier LM, Gonzalez-Rothi EJ, Streeter KA, Posgai SS, Poirier AS, Fuller DD, Reier PJ, Baekey DM (2017) Intraspinal microstimulation and diaphragm activation after cervical spinal cord injury. J Neurophysiol 117:767. https://doi.org/10.1152/jn.00721.2016

Gonzalez-Rothi EJ, Streeter KA, Hanna MH, Stamas AC, Reier PJ, Baekey DM, Fuller DD (2017) High-frequency epidural stimulation across the respiratory cycle evokes phrenic short-term potentiation after incomplete cervical spinal cord injury. J Neurophysiol 118(4):2344–2357. https://doi.org/10.1152/jn.00913.2016

DiMarco AF, Kowalski KE, Geertman RT, Hromyak DR (2006) Spinal cord stimulation: a new method to produce an effective cough in patients with spinal cord injury. Am J Respir Crit Care Med 173:1386–1389. https://doi.org/10.1164/rccm.200601-097CR

DiMarco AF, Kowalski KE, Hromyak DR, Geertman RT (2014) Long-term follow-up of spinal cord stimulation to restore cough in subjects with spinal cord injury. J Spinal Cord Med 37:380–388. https://doi.org/10.1179/2045772313Y.0000000152

Ерохин АН, Кобызев АЕ, Сергеенко ОМ, Туровинина ЕФ (2020) Стимуляция диафрагмального нерва посредством модифицированного имплантируемого устройства в комплексе реабилитационных мероприятий после повреждения шейного отдела спинного мозга (случай из практики). Гений ортопедии 26:89–94 [Erokhin AN, Kobizev AE, Sergeenko OM, Turovinina EF (2020) Phrenic nerve stimulation in complex rehabilitation for cervical spinal cord injury using modified implantable device (case report). Geniy Ortopedii 26(1):89–94. (In Russ)]. DOI1018019/1028-4427-2020-26-1-89-94

Duffin J, Li YM (2006) Transmission of respiratory rhythm: midline-crossing connections at the level of the phrenic motor nucleus? Resp Physiol Neurobiol 153(2):139–147. https://doi.org/10.1016/j.resp.2005.09.011

Tian GF, Duffin J (1996) Spinal connections of ventral-group bulbospinal inspiratory neurons studied with cross-correlation in the decerebrate rat. Exp Brain Res 111(2):178–186. https://doi.org/10.1007/BF00227296

Minyaeva AV, Moiseev SA, Pukhov AM, Savokhin AA, Gerasimenko YP, Moshonkina TR (2017) Response of external inspiration to the movements induced by transcutaneous spinal cord stimulation. Human Physiol 43(5): 524–531. https://doi.org/10.1134/S0362119717050115

Moshonkina TR, Scherbakova NA, Moiseev SA, Minyaeva AV, Gerasimenko YP (2020) Regulation of respiration during electrical stimulation of the lumbar spinal cord in humans. Integrat Physiol 1:108–115. https://doi.org/10.1016/j.mayocp.2017.04.011

Gad P, Kreydin E, Zhong H, Edgerton VR (2020) Spinal Networks and Spinal Cord Injury: A Tribute to Reggie Edgerton: Enabling respiratory control after severe chronic tetraplegia: an exploratory case study. J Neurophysiol 124(3):774. https://doi.org/10.1152/jn.00320.2020

Del Negro CA, Funk GD, Feldman JL (2018) Breathing matters. Nat Rev Neurosci 19(6):351–367. https://doi.org/10.1038/s41583-018-0003-6

Miller J, Eldabe S, Buchser E, Johanek LM, Guan Y, Linderoth B (2016) Parameters of spinal cord stimulation and their role in electrical charge delivery: a review. Neuromodulation: Technology at the Neural Interface 19(4):373–384. https://doi.org/10.1111/ner.12438

Joosten EA, Franken G (2020) Spinal cord stimulation in chronic neuropathic pain: mechanisms of action, new locations, new paradigms. Pain 161(1):S104. https://doi.org/10.1097/j.pain.0000000000001854

Shandybina ND, Kuropatenko MV, Moshonkina TR (2022) Relevance of the transcutaneous spinal cord stimulation for regulation of the external respiration. Motor Control 122.