Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits

Sevda C. Aslan; Bonnie E. Legg Ditterline; Michael C. Park; Claudia A. Angeli; Enrico Rejc; Yangsheng Chen; Alexander V. Ovechkin; Andrei Krassioukov; Susan J. Harkema

doi:10.3389/fphys.2018.00565

Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits

Sevda C. Aslan, Bonnie E. Legg Ditterline, Michael C. Park, Claudia A. Angeli, Enrico Rejc, Yangsheng Chen, Alexander V. Ovechkin, Andrei Krassioukov, Susan J. Harkema

Neurosurgery

Research output: Contribution to journal › Article › peer-review

80 Scopus citations

Abstract

Disruption of motor and autonomic pathways induced by spinal cord injury (SCI) often leads to persistent low arterial blood pressure and orthostatic intolerance. Spinal cord epidural stimulation (scES) has been shown to enable independent standing and voluntary movement in individuals with clinically motor complete SCI. In this study, we addressed whether scES configured to activate motor lumbosacral networks can also modulate arterial blood pressure by assessing continuous, beat-by-beat blood pressure and lower extremity electromyography during supine and standing in seven individuals with C5-T4 SCI. In three research participants with arterial hypotension, orthostatic intolerance, and low levels of circulating catecholamines (group 1), scES applied while supine and standing resulted in increased arterial blood pressure. In four research participants without evidence of arterial hypotension or orthostatic intolerance and normative circulating catecholamines (group 2), scES did not induce significant increases in arterial blood pressure. During scES, there were no significant differences in electromyographic (EMG) activity between group 1 and group 2. In group 1, during standing assisted by scES, blood pressure was maintained at 119/72 ± 7/14 mmHg (mean ± SD) compared with 70/45 ± 5/7 mmHg without scES. In group 2 there were no arterial blood pressure changes during standing with or without scES. These findings demonstrate that scES configured to facilitate motor function can acutely increase arterial blood pressure in individuals with SCI-induced cardiovascular deficits.

Original language	English (US)
Article number	565
Journal	Frontiers in Physiology
Volume	9
Issue number	MAY
DOIs	https://doi.org/10.3389/fphys.2018.00565
State	Published - May 18 2018

Bibliographical note

Funding Information:
We are indebted to our research participants for their courage, dedication, motivation, and perseverance that made these research findings possible. We also gratefully acknowledge Rebekah Morton, Paul Criscola, Matthew Green, and our training staff for their support of the research volunteers; Maxwell Boakye, MD and Jonathan Hodes, MD for surgical procedures; Douglas Stevens, MD, Darryl Kaelin MD, and Yukishia Austin for medical oversight; Andrea Willhite, Christie Ferreira, Samina Mesbah, Dengzhi Wang, and our research staff for their contribution to the data collection and analysis; and Doug Lorenz, PhD for statistical assistance. This work was supported by: The Leona M. and Harry B. Helmsley Charitable Trust, US National Institutes of Health, NIBIB, under the award number R01EB00qIGMS P30 GM103507, Christopher and Dana Reeve Foundation, Kessler Foundation, Kentucky Spinal Cord Injury Research Center, University of Louisville Foundation, and Medtronic Plc.

Publisher Copyright:
© 2018 Aslan, Legg Ditterline, Park, Angeli, Rejc, Chen, Ovechkin, Krassioukov and Harkema.

Keywords

Blood pressure
Epidural stimulation
Human spinal cord injury
Orthostatic hypotension
Systemic hypotension

Publisher link

10.3389/fphys.2018.00565

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5968099

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Aslan, S. C., Legg Ditterline, B. E., Park, M. C., Angeli, C. A., Rejc, E., Chen, Y., Ovechkin, A. V., Krassioukov, A., & Harkema, S. J. (2018). Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits. Frontiers in Physiology, 9(MAY), Article 565. https://doi.org/10.3389/fphys.2018.00565

Aslan, SC, Legg Ditterline, BE, Park, MC, Angeli, CA, Rejc, E, Chen, Y, Ovechkin, AV, Krassioukov, A & Harkema, SJ 2018, 'Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits', Frontiers in Physiology, vol. 9, no. MAY, 565. https://doi.org/10.3389/fphys.2018.00565

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title = "Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits",

abstract = "Disruption of motor and autonomic pathways induced by spinal cord injury (SCI) often leads to persistent low arterial blood pressure and orthostatic intolerance. Spinal cord epidural stimulation (scES) has been shown to enable independent standing and voluntary movement in individuals with clinically motor complete SCI. In this study, we addressed whether scES configured to activate motor lumbosacral networks can also modulate arterial blood pressure by assessing continuous, beat-by-beat blood pressure and lower extremity electromyography during supine and standing in seven individuals with C5-T4 SCI. In three research participants with arterial hypotension, orthostatic intolerance, and low levels of circulating catecholamines (group 1), scES applied while supine and standing resulted in increased arterial blood pressure. In four research participants without evidence of arterial hypotension or orthostatic intolerance and normative circulating catecholamines (group 2), scES did not induce significant increases in arterial blood pressure. During scES, there were no significant differences in electromyographic (EMG) activity between group 1 and group 2. In group 1, during standing assisted by scES, blood pressure was maintained at 119/72 ± 7/14 mmHg (mean ± SD) compared with 70/45 ± 5/7 mmHg without scES. In group 2 there were no arterial blood pressure changes during standing with or without scES. These findings demonstrate that scES configured to facilitate motor function can acutely increase arterial blood pressure in individuals with SCI-induced cardiovascular deficits.",

keywords = "Blood pressure, Epidural stimulation, Human spinal cord injury, Orthostatic hypotension, Systemic hypotension",

author = "Aslan, {Sevda C.} and {Legg Ditterline}, {Bonnie E.} and Park, {Michael C.} and Angeli, {Claudia A.} and Enrico Rejc and Yangsheng Chen and Ovechkin, {Alexander V.} and Andrei Krassioukov and Harkema, {Susan J.}",

note = "Funding Information: We are indebted to our research participants for their courage, dedication, motivation, and perseverance that made these research findings possible. We also gratefully acknowledge Rebekah Morton, Paul Criscola, Matthew Green, and our training staff for their support of the research volunteers; Maxwell Boakye, MD and Jonathan Hodes, MD for surgical procedures; Douglas Stevens, MD, Darryl Kaelin MD, and Yukishia Austin for medical oversight; Andrea Willhite, Christie Ferreira, Samina Mesbah, Dengzhi Wang, and our research staff for their contribution to the data collection and analysis; and Doug Lorenz, PhD for statistical assistance. This work was supported by: The Leona M. and Harry B. Helmsley Charitable Trust, US National Institutes of Health, NIBIB, under the award number R01EB00qIGMS P30 GM103507, Christopher and Dana Reeve Foundation, Kessler Foundation, Kentucky Spinal Cord Injury Research Center, University of Louisville Foundation, and Medtronic Plc. Publisher Copyright: {\textcopyright} 2018 Aslan, Legg Ditterline, Park, Angeli, Rejc, Chen, Ovechkin, Krassioukov and Harkema.",

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doi = "10.3389/fphys.2018.00565",

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AU - Aslan, Sevda C.

AU - Legg Ditterline, Bonnie E.

AU - Park, Michael C.

AU - Angeli, Claudia A.

AU - Rejc, Enrico

AU - Chen, Yangsheng

AU - Ovechkin, Alexander V.

AU - Krassioukov, Andrei

AU - Harkema, Susan J.

N1 - Funding Information: We are indebted to our research participants for their courage, dedication, motivation, and perseverance that made these research findings possible. We also gratefully acknowledge Rebekah Morton, Paul Criscola, Matthew Green, and our training staff for their support of the research volunteers; Maxwell Boakye, MD and Jonathan Hodes, MD for surgical procedures; Douglas Stevens, MD, Darryl Kaelin MD, and Yukishia Austin for medical oversight; Andrea Willhite, Christie Ferreira, Samina Mesbah, Dengzhi Wang, and our research staff for their contribution to the data collection and analysis; and Doug Lorenz, PhD for statistical assistance. This work was supported by: The Leona M. and Harry B. Helmsley Charitable Trust, US National Institutes of Health, NIBIB, under the award number R01EB00qIGMS P30 GM103507, Christopher and Dana Reeve Foundation, Kessler Foundation, Kentucky Spinal Cord Injury Research Center, University of Louisville Foundation, and Medtronic Plc. Publisher Copyright: © 2018 Aslan, Legg Ditterline, Park, Angeli, Rejc, Chen, Ovechkin, Krassioukov and Harkema.

PY - 2018/5/18

Y1 - 2018/5/18

N2 - Disruption of motor and autonomic pathways induced by spinal cord injury (SCI) often leads to persistent low arterial blood pressure and orthostatic intolerance. Spinal cord epidural stimulation (scES) has been shown to enable independent standing and voluntary movement in individuals with clinically motor complete SCI. In this study, we addressed whether scES configured to activate motor lumbosacral networks can also modulate arterial blood pressure by assessing continuous, beat-by-beat blood pressure and lower extremity electromyography during supine and standing in seven individuals with C5-T4 SCI. In three research participants with arterial hypotension, orthostatic intolerance, and low levels of circulating catecholamines (group 1), scES applied while supine and standing resulted in increased arterial blood pressure. In four research participants without evidence of arterial hypotension or orthostatic intolerance and normative circulating catecholamines (group 2), scES did not induce significant increases in arterial blood pressure. During scES, there were no significant differences in electromyographic (EMG) activity between group 1 and group 2. In group 1, during standing assisted by scES, blood pressure was maintained at 119/72 ± 7/14 mmHg (mean ± SD) compared with 70/45 ± 5/7 mmHg without scES. In group 2 there were no arterial blood pressure changes during standing with or without scES. These findings demonstrate that scES configured to facilitate motor function can acutely increase arterial blood pressure in individuals with SCI-induced cardiovascular deficits.

AB - Disruption of motor and autonomic pathways induced by spinal cord injury (SCI) often leads to persistent low arterial blood pressure and orthostatic intolerance. Spinal cord epidural stimulation (scES) has been shown to enable independent standing and voluntary movement in individuals with clinically motor complete SCI. In this study, we addressed whether scES configured to activate motor lumbosacral networks can also modulate arterial blood pressure by assessing continuous, beat-by-beat blood pressure and lower extremity electromyography during supine and standing in seven individuals with C5-T4 SCI. In three research participants with arterial hypotension, orthostatic intolerance, and low levels of circulating catecholamines (group 1), scES applied while supine and standing resulted in increased arterial blood pressure. In four research participants without evidence of arterial hypotension or orthostatic intolerance and normative circulating catecholamines (group 2), scES did not induce significant increases in arterial blood pressure. During scES, there were no significant differences in electromyographic (EMG) activity between group 1 and group 2. In group 1, during standing assisted by scES, blood pressure was maintained at 119/72 ± 7/14 mmHg (mean ± SD) compared with 70/45 ± 5/7 mmHg without scES. In group 2 there were no arterial blood pressure changes during standing with or without scES. These findings demonstrate that scES configured to facilitate motor function can acutely increase arterial blood pressure in individuals with SCI-induced cardiovascular deficits.

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KW - Human spinal cord injury

KW - Orthostatic hypotension

KW - Systemic hypotension

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Epidural spinal cord stimulation of lumbosacral networks modulates arterial blood pressure in individuals with spinal cord injury-induced cardiovascular deficits

Abstract

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