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Cardiovascular Consequences of Estrogen Deficiency: Studies in Premenopausal Women

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Cardiovascular Consequences of Estrogen Deficiency: Studies in Premenopausal Women Cardiovascular Consequences of Estrogen Deficiency: Studies in Premenopausal Women by Emma O'Donnell A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Exercise Sciences University of Toronto © Copyright by Emma O'Donnell 2013 Cardiovascular Consequences of Estrogen Deficiency: Studies in Premenopausal Women Emma O’Donnell Doctor of Philosophy Graduate Department of Exercise Sciences University of Toronto 2013 Abstract The influence of estrogen deficiency in physically active women with functional hypothalamic amenorrhea (ExFHA) on cardiovascular regulation is unknown. Three mechanistic studies compared cardiovascular responses to exercise and orthostatic stress in ExFHA women with responses in physically active (ExOv) and sedentary (SedOv) eumenorrheic ovulatory women. Measures included calf blood flow (BF), brachial artery (BA) endothelial dependent and independent function, shear rate (SR), vascular resistance (VR), blood pressure (BP), heart rate (HR), HR variability (HRV), muscle sympathetic nervous activity (MSNA), and serum renin- angiotensin-aldosterone system (RAAS) components. Study one examined the effects of a single bout of dynamic exercise on vascular function in ExFHA (n=12), ExOv (n=14), and SedOv (n=15) women. Pre-exercise, calf BF and BA endothelium-dependent flow-mediated vasodilation (FMD%) were lower (p<0.05) in ExFHA versus ovulatory women in association with higher (p<0.05) calf VR and lower (p<0.05) SR, respectively. Endothelium-independent vasodilation, assessed at baseline only, was also lower (p<0.05) in ExFHA. Post-exercise, calf BF was increased and VR decreased ii (p<0.05) in ExFHA women, similar (p>0.05) to that observed in ovulatory women. FMD% and SR were augmented (p<0.05) post-exercise, but both remained lower (p<0.05) in ExFHA versus ovulatory women (p<0.05). Study two investigated neurohumoral (MSNA and RAAS) BP regulation during orthostatic stress in ExFHA (n=12) and ExOv (n=17) women. Baseline systolic BP was lower (p<0.05) in ExFHA versus ExOv. Neurohumoral measures did not differ (p>0.05) between the groups at baseline. However, during hypotensive stimuli, MSNA increased to a greater extent (p<0.05), yet angiotensin II and renin were not activated in ExFHA women. Study three examined autonomic control of HR during orthostatic stress in ExFHA (n=11), ExOv (n=17), and SedOv (n=17) women. Lower HR (p<0.05) at rest and during orthostatic stress in ExFHA was associated with markedly elevated (p<0.05) HRV due to higher (p<0.05) parasympathetic modulation. Sympathetic modulation did not differ (p>0.05) between the groups. These studies indicate altered cardiovascular regulation in otherwise healthy ExFHA women. The influence of estrogen deficiency per se in these alterations are not clear, but in light of the etiology of amenorrhea, it is likely that complex interactions between estrogen and energy deficiency and exercise training are involved. iii Acknowledgements I would like to dedicate this thesis to my husband. My partner in life and my rock. Your love and companionship throughout this entire academic journey gave me immense strength. I could not have done this without your support and understanding. This research could not have been possible without the many participants who gave so much of their time and effort. I enjoyed meeting each and every one of you. It was truly my pleasure to have crossed paths with so many interesting women. Thank you all. During all three studies, which were conducted at the Toronto General Hospital in the Clinical Cardiovascular Regulation Laboratory, there were several people that were instrumental in making this research a success. The facility itself was generously made available to me by Dr John Floras, who I'd like to thank for providing me the opportunity to learn unique laboratory skills and to conduct my research in such a positive environment. For Study Two, Dr Hisa Murai gave much of his time and expertise by performing microneurography in many of my participants. I can't thank you enough for your perseverance and dedication in obtaining such high quality data on my behalf. Bev Morris (RN), you made the long study days so much more bearable and enjoyable, both for me and my participants. Your assistance in each and every single study was always appreciated, but the wonderful manner with which you welcomed and greeted my participants made each and every one of them actually want to come back to complete the next study visit. Thank you. Thanks go to my friends, Andrea, Susan, Leanna, Kerry and Jane who have been genuinely interested in my research and have been gracious enough to listen to me talk about the same topic for the last 6 years! I love you all dearly. A heartfelt thanks also goes to my fellow students, Steve, Danielle, Marc, Ming and Sam. You are all so talented and I'm going to miss you! I look forward to our paths crossing again in the not too distant future. I would like to gratefully thank my committee members for their time and efforts. Your input was highly valued and contributed importantly to my academic success. iv Special thanks go to my two supervisors, Dr Jack Goodman and Dr Paula Harvey. I was truly fortunate to have two such dedicated individuals to guide me through this process. Jack, thank you for giving me the opportunity to pursue my academic goals. You were always so supportive and encouraging. I will miss our conversations. Paula, thank you for investing in me. The support, time and energy you gave me was so generous and so very much appreciated. The level of excellence that you have engendered in me will place me in good stead for all my future endeavours. v Table of Contents Page Abstract.............................................................................................................................. ii Acknowledgements............................................................................................................ iv Table of Contents............................................................................................................... vi List of Tables...................................................................................................................... x List of Figures.................................................................................................................... xi List of Appendices.............................................................................................................. xiii List of Abbreviations.......................................................................................................... xiv CHAPTER 1: INTRODUCTION...................................................................................... 1 1. 1 Overview................................................................................................................. 1 1.2 Organization of the Thesis...................................................................................... 3 1.3 Experimental Hypotheses and Purposes................................................................. 6 1.3.1 Study One........................................................................................................ 7 1.3.2 Study Two....................................................................................................... 8 1.3.3 Study Three..................................................................................................... 9 CHAPTER 2: REVIEW OF LITERATURE..................................................................... 10 2.1 Introduction............................................................................................................. 10 2.2 Definitions.............................................................................................................. 11 2.3 Estrogen Synthesis, Sources, Metabolism and Receptors...................................... 12 2.3.1 Estrogen Biosynthetic Pathway and Sources................................................... 12 2.3.2 Estrogen Transport and Metabolism............................................................... 15 2.3.3 Estrogen Receptors: Distribution, Expression and Regulation....................... 16 2.4 Vascular Function.................................................................................................. 19 2.4.1 Endothelium and Endothelial Function........................................................... 19 2.4.2 Endothelial Dysfunction................................................................................. 20 2.4.3 Nitric Oxide..................................................................................................... 20 2.5 Effects of Estrogen on the Vasculature.................................................................. 23 vi 2.5.1 Non-genomic Effects....................................................................................... 23 2.5.2 Genomic Effects.............................................................................................. 24 2.5.3 Other Effects of Estrogen on Vasoregulation.................................................. 25 2.6 Effects of Acute and Chronic Exercise on the Endothelium................................... 26 2.6.1 Shear Stress....................................................................................................... 26 2.6.1.1 Mechanotransduction of Shear Stress........................................................ 28 2.6.1.2 Acute versus Chronic Shear Stress Activation: Flow Mediated
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