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December 10, 2019; 93 (24) Article

Sleep-disordered breathing is associated with brain vascular reactivity in spinal cord injury

Jordan W. Squair, Amanda H.X. Lee, Zoe K. Sarafis, Geoff Coombs, Otto Barak, Jacquelyn J. Cragg, Tanja Mijacika, Renata Pecotic, Andrei V. Krassioukov, Zoran Dogas, Zeljko Dujic, Aaron A. Phillips
First published November 6, 2019, DOI: https://doi.org/10.1212/WNL.0000000000008619
Jordan W. Squair
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Amanda H.X. Lee
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Zoe K. Sarafis
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Geoff Coombs
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Otto Barak
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Jacquelyn J. Cragg
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Tanja Mijacika
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Renata Pecotic
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Andrei V. Krassioukov
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Zoran Dogas
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Zeljko Dujic
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Aaron A. Phillips
From the Departments of Physiology and Pharmacology, Clinical Neurosciences, and Cardiac Sciences (J.W.S., A.A.P.), and Hotchkiss Brain Institute, Libin Cardiovascular Institute of Alberta, Cumming School of Medicine (J.W.S., A.A.P.), University of Calgary; Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development (G.C.), University of British Columbia Okanagan, Kelowna; International Collaboration on Repair Discoveries (ICORD) (J.W.S., A.H.X.L., Z.K.S., J.J.C., A.V.K.), MD/PhD Training Program (J.W.S.), and Department of Experimental Medicine (J.W.S., A.H.X.L.), Faculty of Medicine, and Faculty of Pharmaceutical Sciences (J.J.C.), University of British Columbia, Vancouver, Canada; Department of Integrative Physiology (O.B., T.M., Z.D.) and Department of Neuroscience, Split Sleep Medicine Center (R.P., Z.D.), University of Split School of Medicine, Split, Croatia; and Department of Physiology (O.B.), University of Novi Sad Medical School, Serbia.
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Citation
Sleep-disordered breathing is associated with brain vascular reactivity in spinal cord injury
Jordan W. Squair, Amanda H.X. Lee, Zoe K. Sarafis, Geoff Coombs, Otto Barak, Jacquelyn J. Cragg, Tanja Mijacika, Renata Pecotic, Andrei V. Krassioukov, Zoran Dogas, Zeljko Dujic, Aaron A. Phillips
Neurology Dec 2019, 93 (24) e2181-e2191; DOI: 10.1212/WNL.0000000000008619

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Abstract

Objective To determine the population-level odds of individuals with spinal cord injury (SCI) experiencing fatigue and sleep apnea, to elucidate relationships with level and severity of injury, and to examine associations with abnormal cerebrovascular responsiveness.

Methods We used population-level data, meta-analyses, and primary physiologic assessments to provide a large-scale integrated assessment of sleep-related complications after SCI. Population-level and meta-analyses included more than 60,000 able-bodied individuals and more than 1,800 individuals with SCI. Physiologic assessments were completed on a homogenous sample of individuals with cervical SCI and matched controls. We examined the prevalence of (1) self-reported chronic fatigue, (2) clinically identified sleep apnea, and 3) cerebrovascular responsiveness to changing CO2.

Results Logistic regression revealed a 7-fold elevated odds of chronic fatigue after SCI (odds ratio [OR] 7.9, 95% confidence interval [CI] 3.5–16.2), and that fatigue and trouble sleeping are correlated with the level and severity of injury. We further show that those with SCI experience elevated risk of clinically defined sleep-disordered breathing in more than 600 individuals with SCI (pooled OR 3.1, 95% CI 1.3–7.5). We confirmed that individuals with SCI experience a high rate of clinically defined sleep apnea using primary polysomnography assessments. We then provide evidence using syndromic analysis that sleep-disordered breathing is a factor strongly associated with impaired cerebrovascular responsiveness to CO2 in patients with SCI.

Conclusions Individuals with SCI have an increased prevalence of sleep-disordered breathing, which may partially underpin their increased risk of stroke. There is thus a need to integrate sleep-related breathing examinations into routine care for individuals with SCI.

Glossary

AB=
able-bodied;
AHI=
apnea–hypopnea index;
AIS=
American Spinal Injury Association Impairment Scale;
BMI=
body mass index;
CCHS=
Canadian Community Health Survey;
CI=
confidence interval;
MCA=
middle cerebral artery;
OR=
odds ratio;
PCA=
posterior cerebral artery;
SCI=
spinal cord injury;
SCICS=
SCI Community Survey;
SDB=
sleep-disordered breathing

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • CME Course: NPub.org/cmelist

  • Received March 4, 2019.
  • Accepted in final form June 20, 2019.
  • © 2019 American Academy of Neurology
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