Epidural Spinal Cord Stimulation of Lumbosacral Networks Modulates Arterial Blood Pressure in Individuals With Spinal Cord Injury-Induced Cardiovascular Deficits

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.

[1]  S. Harkema,et al.  Normalization of Blood Pressure With Spinal Cord Epidural Stimulation After Severe Spinal Cord Injury , 2018, Front. Hum. Neurosci..

[2]  B. C. Craven,et al.  Cardiovascular disease risk in individuals with chronic spinal cord injury: Prevalence of untreated risk factors and poor adherence to treatment guidelines , 2018, The journal of spinal cord medicine.

[3]  J. Taylor,et al.  Baroreflex autonomic control in human spinal cord injury: Physiology, measurement, and potential alterations , 2017, Autonomic Neuroscience.

[4]  W. Bauman,et al.  Implication of altered autonomic control for orthostatic tolerance in SCI , 2017, Autonomic Neuroscience.

[5]  S. Harkema,et al.  Motor recovery after activity-based training with spinal cord epidural stimulation in a chronic motor complete paraplegic , 2017, Scientific Reports.

[6]  Enrico Rejc,et al.  Effects of Stand and Step Training with Epidural Stimulation on Motor Function for Standing in Chronic Complete Paraplegics. , 2017, Journal of neurotrauma.

[7]  S. Harkema,et al.  Effects of Lumbosacral Spinal Cord Epidural Stimulation for Standing after Chronic Complete Paralysis in Humans , 2015, PloS one.

[8]  M. Fehlings,et al.  Acute Spinal Cord Injury , 2015, Journal of spinal disorders & techniques.

[9]  A. Krassioukov,et al.  Nonpharmacologic management of orthostatic hypotension: a systematic review. , 2015, Archives of physical medicine and rehabilitation.

[10]  S. Harkema,et al.  Altering spinal cord excitability enables voluntary movements after chronic complete paralysis in humans. , 2014, Brain : a journal of neurology.

[11]  L. Chan,et al.  Incidence, prevalence, costs, and impact on disability of common conditions requiring rehabilitation in the United States: stroke, spinal cord injury, traumatic brain injury, multiple sclerosis, osteoarthritis, rheumatoid arthritis, limb loss, and back pain. , 2014, Archives of physical medicine and rehabilitation.

[12]  D. Tulsky,et al.  Impact of blood pressure dysregulation on health-related quality of life in persons with spinal cord injury: development of a conceptual model. , 2013, Archives of physical medicine and rehabilitation.

[13]  Andrei Krassioukov,et al.  International standards for neurological classification of spinal cord injury, revised 2011. , 2012, Topics in spinal cord injury rehabilitation.

[14]  Christie K. Ferreira,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 , 2011, The Lancet.

[15]  Jens Jordan,et al.  Consensus statement on the definition of orthostatic hypotension, neurally mediated syncope and the postural tachycardia syndrome , 2011, Clinical Autonomic Research.

[16]  J. Handrakis,et al.  Effects of midodrine hydrochloride on blood pressure and cerebral blood flow during orthostasis in persons with chronic tetraplegia. , 2010, Archives of physical medicine and rehabilitation.

[17]  A. Krassioukov,et al.  A systematic review of the management of orthostatic hypotension after spinal cord injury. , 2009, Archives of physical medicine and rehabilitation.

[18]  N. Hjeltnes,et al.  Non-pharmacological management of orthostatic hypotension after spinal cord injury: a critical review of the literature , 2008, Spinal Cord.

[19]  R. Freeman Current pharmacologic treatment for orthostatic hypotension , 2008, Clinical Autonomic Research.

[20]  D. Euler,et al.  Acute cardiovascular effects of epidural spinal cord stimulation. , 2007, Pain physician.

[21]  J. Weir,et al.  Blunted heart rate response to vagal withdrawal in persons with tetraplegia , 2006, Clinical Autonomic Research.

[22]  J. Steeves,et al.  Orthostatic hypotension following spinal cord injury: understanding clinical pathophysiology , 2006, Spinal Cord.

[23]  Fumiyasu Yamasaki,et al.  Artificial Baroreflex: Clinical Application of a Bionic Baroreflex System , 2006, Circulation.

[24]  G. Cheing,et al.  The effects of lower-extremity functional electric stimulation on the orthostatic responses of people with tetraplegia. , 2005, Archives of physical medicine and rehabilitation.

[25]  D. Pegelow,et al.  Skeletal muscle pump versus respiratory muscle pump: modulation of venous return from the locomotor limb in humans , 2005, The Journal of physiology.

[26]  M. Sugimachi,et al.  Bionic epidural stimulation restores arterial pressure regulation during orthostasis. , 2004, Journal of applied physiology.

[27]  S. Hinderer,et al.  Double-Blinded, Placebo-Controlled Trial Of Midodrine For Exercise Performance Enhancement In Tetraplegia:A Pilot Study , 2004, The journal of spinal cord medicine.

[28]  A. Krassioukov,et al.  Descending vasomotor pathways in humans: correlation between axonal preservation and cardiovascular dysfunction after spinal cord injury. , 2003, Journal of neurotrauma.

[29]  P. Jacobs,et al.  Physiologic Responses To Electrically Assisted And Frame-Supported Standing In Persons With Paraplegia , 2003, The journal of spinal cord medicine.

[30]  P. Faghri,et al.  Electrically induced and voluntary activation of physiologic muscle pump: a comparison between spinal cord-injured and able-bodied individuals , 2002, Clinical rehabilitation.

[31]  A. Rice,et al.  Mechanisms of neuropathic pain. , 2001, British journal of anaesthesia.

[32]  K. Stiller,et al.  The prevalence of orthostatic hypotension during physiotherapy treatment in patients with an acute spinal cord injury , 2000, Spinal Cord.

[33]  R. Shields,et al.  Effect of functional neuromuscular stimulation on postural related orthostatic stress in individuals with acute spinal cord injury. , 2000, Journal of rehabilitation research and development.

[34]  R. Vaglienti,et al.  Spinal Cord Stimulation in Severe, Inoperable Peripheral Vascular Disease , 2000, Neuromodulation : journal of the International Neuromodulation Society.

[35]  A. Krassioukov,et al.  Cardiovascular consequences of loss of supraspinal control of the sympathetic nervous system after spinal cord injury. , 2000, Archives of physical medicine and rehabilitation.

[36]  B J Andrews,et al.  Functional electrical stimulation effect on orthostatic hypotension after spinal cord injury. , 2000, Archives of physical medicine and rehabilitation.

[37]  F. Fouad-Tarazi,et al.  Usefulness of Plasma Catecholamines During Head‐Up Tilt as a Measure of Sympathetic Activation in Vasovagal Patients , 1998, Pacing and clinical electrophysiology : PACE.

[38]  P. Persson,et al.  Frequency-response characteristics of autonomic nervous system function in conscious rats. , 1997, The American journal of physiology.

[39]  J. Blackmer,et al.  Orthostatic hypotension in spinal cord injured patients. , 1997, The journal of spinal cord medicine.

[40]  K H Wesseling,et al.  Reconstruction of brachial artery pressure from noninvasive finger pressure measurements. , 1996, Circulation.

[41]  J K Triedman,et al.  Blood pressure modulation by central venous pressure and respiration. Buffering effects of the heart rate reflexes. , 1994, Circulation.

[42]  J. Miles,et al.  Spinal cord stimulation in peripheral vascular disease. , 1992, British journal of neurosurgery.

[43]  R. Pawl Spinal cord stimulation. , 2020, The Clinical journal of pain.

[44]  D. Slaaf,et al.  Epidural Spinal Cord Electrical Stimulation Improves Microvascular Blood Flow in Severe Limb Ischemia , 1988, Annals of surgery.

[45]  L. Illis,et al.  Spinal cord stimulation in peripheral vascular disease. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[46]  J. Gillespie,et al.  A method of stimulating the complete sympathetic outflow from the spinal cord to blood vessels in the pithed rat. , 1967, British journal of pharmacology and chemotherapy.

[47]  E. A. Stead,et al.  Cardiac output in man; an analysis of the mechanisms varying the cardiac output based on recent clinical studies. , 1947, Archives of internal medicine.