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Cardiovascular Disease Risk after Spinal Cord Injury: The Role of Autonomic Dysfunction PDF

140 Pages·2013·10.43 MB·English
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Cardiovascular Disease Risk after Spinal Cord Injury: The Role of Autonomic Dysfunction by Henrike Joanna Cornelie (Rianne) Ravensbergen M.Sc., Free University Amsterdam, 2005 Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Department of Biomedical Physiology and Kinesiology Faculty of Science © Henrike Joanna Cornelie (Rianne) Ravensbergen 2013 SIMON FRASER UNIVERSITY Summer 2013 Approval Name: Henrike Joanna Cornelie (Rianne) Ravensbergen Degree: Doctor of Philosophy Title of Thesis: Cardiovascular Disease Risk after Spinal Cord Injury: The Role of Autonomic Dysfunction Examining Committee: Chair: Angela Brooks-Wilson Associate Professor Victoria Claydon Senior Supervisor Assistant Professor Department of Biomedical Physiology and Kinesiology Scott Lear Supervisor Professor Department of Biomedical Physiology and Kinesiology Shubhayan Sanatani Supervisor Associate Professor Department of Pediatrics Faculty of Medicine, University of British Columbia Will Cupples Internal Examiner Professor Department of Biomedical Physiology and Kinesiology Vaughan Macefield External Examiner Professor School of Medicine University of Western Sydney Date Defended/Approved: August 7, 2013 ii Partial Copyright Licence iii Abstract Cardiovascular disease (CVD) is the leading cause for mortality and morbidity in those with spinal cord injury (SCI), with an earlier onset and more rapid progression compared to the general population. Lifestyle changes after injury have been suggested to be the main contributor to CVD risk, but I proposed that the issue is more complicated. Although less well-known, autonomic function is affected by SCI, in addition to motor and sensory dysfunction. Cardiovascular autonomic dysfunction is a particular concern in individuals with high lesions (above T5) due to the possible disruption of descending spinal sympathetic pathways to the heart and main vascular resistance bed. In this thesis, I propose that cardiovascular autonomic impairment plays a role in the elevated CVD risk. The thesis starts with an evaluation of the prevalence and progression of cardiovascular dysfunction after SCI. Then, the contribution of autonomic dysfunction on CVD risk is investigated. In addition, markers for obesity-related CVD risk specific to individuals with SCI and ECG markers for cardiac arrhythmias in relation to autonomic impairments are explored. Prevalence of cardiovascular dysfunction was found not to improve over time after injury and it was highest in those with lesions above T5. The second study showed that autonomic dysfunction contributes to overall CVD risk and specifically to glucose intolerance, either directly or through an interaction with physical activity levels. The data showed that waist circumference is the best marker for obesity considering ability to detect adiposity and CVD risk, and practicality of use. A specific cut-off for waist circumference was found to be lower compared to the general recommendations. The final study showed increased values for the ECG markers Tpeak- Tend variability, P-wave variability and QT variability index, only in those with impairments to descending cardiac sympathetic pathways. The ECG characteristics may be indicative of susceptibility to cardiac arrhythmia related to autonomic dysfunction. Implications of these findings are that management of cardiovascular autonomic dysfunction should remain a priority into the chronic phase of injury, not merely due the direct impact on quality of life, but also due to its contribution to the elevated cardiovascular disease risk after SCI. Keywords: Spinal cord injury; autonomic nervous system; cardiovascular disease risk; obesity; cardiac arrhythmia; autonomic dysfunction iv Acknowledgements Four years of work went into my Ph.D. thesis, but I could not have done this all by myself. Therefore, I would like to take this opportunity to thank those people who in one way or another helped me to complete this journey. First and foremost I would like to thank all the participants who volunteered their time for the different studies. They are the ones who made this research possible. We had some wonderful conversations during the two hour-long glucose tolerance tests; I learned lots from each and every one of you! Then my senior supervisor, Victoria: many thanks for the chance you gave me to start my Ph.D. program in your lab, when I just moved to Vancouver. We worked closely together both in the lab running the research studies and in teaching KIN 444. Thank you for your guidance and support. I’m looking forward to continuing our collaboration in the future. My supervisory committee members, Scott Lear, Shubhayan Sanatani and Tom Claydon are the next on my list to thank for their support. Your diverse backgrounds lead to stimulating meetings about my project that gave me new inspiration to continue to improve my research. This journey would not have been the same without my lab mates! I’ve always been happy to come into the lab, go for our daily coffee run and be able to pick each other’s brains about all our projects. We had great fun at conferences and both inside and outside lab (mostly during sporting adventures: skiing, cycling, climbing and scuba diving). You’ve all become great friends! Now I’d like to switch to Dutch to thank my family for their support. Dank jullie wel voor alle steun voor mijn keuze naar Vancouver te gaan en het vertrouwen dat jullie in mij hadden, ook al had ik dat soms niet. Ik vond het geweldig de afsluiting van deze 4 jaar (mijn verdediging) samen met jullie te kunnen meemaken! And last but not at all least: Mark, dank je wel lief, in de eerste plaats dat je me hebt meegenomen naar Vancouver. We hebben hier samen en met lieve nieuwe vrienden een geweldige tijd mogen beleven! Bedankt ook voor je steun en vertrouwen in mij en je scherpe blik op mijn onderzoek, waardoor ik het nog beter kon maken. Succes nu met jouw laatste loodjes en dan op naar een mooi nieuw avontuur samen! v Table of Contents Approval .................................................................................................................. ii   Partial Copyright Licence .......................................................................................... iii   Abstract .................................................................................................................. iv   Acknowledgements ................................................................................................... v   Table of Contents .................................................................................................... vi   List of Tables ............................................................................................................ x   List of Figures .......................................................................................................... xi   List of Acronyms ...................................................................................................... xii   Chapter 1. Background ...................................................................................... 1   Spinal cord injury ...................................................................................................... 1   Incidence in Canada ......................................................................................... 2   Care and cure .................................................................................................. 3   Secondary complications of spinal cord injury ..................................................... 5   Autonomic function after spinal cord injury ................................................................. 7   Autonomic pathways ......................................................................................... 8   Cardiovascular autonomic pathways ......................................................... 10   Effects of spinal cord injury on cardiovascular autonomic pathways .................... 11   Acute effects on cardiovascular autonomic control .................................... 12   Arterial baroreflex and blood pressure control ..................................... 12   Adaptations to cardiovascular autonomic pathways ................................... 13   Consequences for cardiovascular function ........................................................ 15   Altered cardiac function .......................................................................... 15   Consequences of altered blood pressure control ....................................... 15   Low supine blood pressure ................................................................. 15   Orthostatic hypotension ..................................................................... 16   Autonomic dysreflexia ....................................................................... 18   Impaired blood pressure responses to exercise .................................... 21   Assessment of autonomic function after injury .................................................. 22   Plasma noradrenaline ............................................................................. 23   Muscle sympathetic nerve activity ............................................................ 23   Sympathetic skin responses ..................................................................... 24   Cutaneous vasomotor responses ............................................................. 24   Heart rate and blood pressure variability .................................................. 25   Relationship between cardiovascular autonomic dysfunction and cardiovascular disease risk .................................................................................................... 26   Consequences of autonomic dysreflexia ........................................................... 26   Elevated risk of cardiac arrhythmias ................................................................. 27   Interaction effects between autonomic dysfunction and lifestyle ........................ 29   Obesity and obesity-related cardiovascular disease risk factors .................. 30   Outline of this thesis ............................................................................................... 32   vi Chapter 2. Prevalence and progression of cardiovascular dysfunction after spinal cord injury ............................................................... 33   Introduction ........................................................................................................... 33   Methods ................................................................................................................. 34   Participants .................................................................................................... 34   Design ........................................................................................................... 35   Cardiovascular parameters .............................................................................. 35   Personal and lesion characteristics ................................................................... 36   Statistical analyses .......................................................................................... 37   Results ................................................................................................................... 38   Participants .................................................................................................... 38   Time course and determinants of systolic and diastolic arterial pressure ............. 40   Time course and determinants of resting and peak heart rate ............................ 42   Prevalence of hypotension ............................................................................... 44   Prevalence of bradycardia, elevated heart rate, and tachycardia ........................ 44   Discussion .............................................................................................................. 46   Strengths and limitations ................................................................................. 50   Conclusion ............................................................................................................. 51   Chapter 3. Complex relationships between autonomic dysfunction, lifestyle changes and cardiovascular disease risk ...................... 53   Introduction ........................................................................................................... 53   Methods ................................................................................................................. 55   Participants .................................................................................................... 55   Measurements of severity of injury .................................................................. 56   Standard neurological classification .......................................................... 56   Cardiovascular autonomic impairment ...................................................... 56   Plasma noradrenaline ........................................................................ 57   Systolic arterial pressure variability analysis ........................................ 57   Cardiovascular disease risk factors ................................................................... 58   Heart rate variability ............................................................................... 58   Blood lipid profiles, insulin and glucose levels ........................................... 58   Oral glucose tolerance ............................................................................ 59   Framingham 30-year risk for cardiovascular disease score ......................... 59   Physical activity level .............................................................................. 59   Body composition ................................................................................... 60   Statistical analyses .......................................................................................... 60   Results ................................................................................................................... 61   Participant characteristics ................................................................................ 61   Group differences in cardiovascular risk factors ................................................. 62   Multiple linear regression models for cardiovascular risk factors ......................... 64   Discussion .............................................................................................................. 67   Strengths and limitations ................................................................................. 70   Conclusion ............................................................................................................. 71   vii Chapter 4. Waist circumference is the best index for obesity-related cardiovascular disease risk in individuals with spinal cord injury .......................................................................................... 72   Introduction ........................................................................................................... 72   Methods ................................................................................................................. 74   Participants .................................................................................................... 74   Anthropometric variables ................................................................................. 75   Body composition ........................................................................................... 75   Fasting plasma levels of lipids, glucose and insulin ............................................ 76   Oral glucose tolerance test .............................................................................. 76   Framingham 30-year risk for cardiovascular disease score ................................. 76   Statistical analyses .......................................................................................... 77   Results ................................................................................................................... 77   Participants .................................................................................................... 77   Anthropometric measures and body composition .............................................. 77   Anthropometric measures and cardiovascular disease risk factors ...................... 78   Anthropometric measures and the Framingham 30-year risk score ..................... 80   Discussion .............................................................................................................. 82   Conclusion ............................................................................................................. 86   Chapter 5. Electrocardiogram-based predictors for cardiac arrhythmia are related to autonomic impairment after spinal cord injury .......................................................................................... 87   Introduction ........................................................................................................... 87   Methods ................................................................................................................. 89   Participants .................................................................................................... 89   Measures of completeness of injury ................................................................. 89   Motor and sensory impairment ................................................................ 89   Autonomic impairment ............................................................................ 89   Sympathetic skin responses ............................................................... 90   Plasma noradrenaline levels ............................................................... 90   Low frequency power of systolic arterial pressure ................................ 91   Continuous electrocardiogram ......................................................................... 91   Electrocardiogram interval detection ........................................................ 91   Variability analyses ................................................................................. 92   12-lead electrocardiogram ............................................................................... 93   Statistics ........................................................................................................ 93   Results ................................................................................................................... 93   Participant characteristics ................................................................................ 94   Continuous electrocardiogram ......................................................................... 94   Electrocardiogram interval analyses ......................................................... 94   Variability analyses ................................................................................. 95   Correlations with autonomic impairment .................................................. 98   12-lead electrocardiogram ............................................................................... 98   Discussion ............................................................................................................ 100   Conclusion ........................................................................................................... 102   viii Chapter 6. General discussion ....................................................................... 103   Prevalence and progression of cardiovascular autonomic dysfunction after spinal cord injury ................................................................................................... 103   Role of autonomic impairment on cardiovascular disease risk ................................... 104   Obesity indices specific for individuals with spinal cord injury ................................... 106   Cardiac arrhythmias and autonomic function ........................................................... 107   Implications and future directions .......................................................................... 108   References ..................................................................................................... 110   Appendix. List of publications arising from this thesis ................................. 127     ix List of Tables Table 2.1.  Participant characteristics ....................................................................... 38   Table 2.2.  Cardiovascular variables at all test occasions according to lesion level ....... 39   Table 2.3.   Blood pressure and heart rate regression analyses results ........................ 42   Table 2.4.  Prevalence of hypotension, bradycardia, elevated heart rate and tachycardia at all test occasions according to lesion level .......................... 45   Table 2.5.   Prevalence of hypotension, bradycardia and elevated heart rate regression analyses ................................................................................ 46   Table 3.1.  Participant characteristics ....................................................................... 62   Table 3.2.   Cardiovascular disease risk factor regression analyses results ................... 66   Table 4.1.  Participant characteristics. ...................................................................... 78   Table 4.2.  Correlations between anthropometric variables and individual risk factors .................................................................................................. 80   Table 5.1.  Participant characteristics. ...................................................................... 94   Table 5.2.  ECG intervals: RRI, QT, QT , T -T and P-wave duration. ..................... 95   c peak end Table 5.3.  Variability parameters: T -T , QTVI and P-wave variability. .................. 98   peak end x

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two cases of SCI were reported in the Egyptian Edwin Smith papyrus. The condition was determined as “an ailment not to be treated”, and thus most Recordings were made using an analog-to-digital converter (Powerlab. 16/30, AD Instruments, Colorado Springs, CO) with a sampling frequency of 1
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