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Characterization, Prevalence, and Risk Factors of Spontaneous And Louisiana State University LSU Digital Commons LSU Doctoral Dissertations Graduate School 2013 Characterization, prevalence, and risk factors of spontaneous and experimental atherosclerosis and vascular imaging in psittaciformes Hugues Beaufrère Louisiana State University and Agricultural and Mechanical College, [email protected] Follow this and additional works at: https://digitalcommons.lsu.edu/gradschool_dissertations Part of the Veterinary Medicine Commons Recommended Citation Beaufrère, Hugues, "Characterization, prevalence, and risk factors of spontaneous and experimental atherosclerosis and vascular imaging in psittaciformes" (2013). LSU Doctoral Dissertations. 1598. https://digitalcommons.lsu.edu/gradschool_dissertations/1598 This Dissertation is brought to you for free and open access by the Graduate School at LSU Digital Commons. It has been accepted for inclusion in LSU Doctoral Dissertations by an authorized graduate school editor of LSU Digital Commons. For more information, please [email protected]. CHARACTERIZATION, PREVALENCE, AND RISK FACTORS OF SPONTANEOUS AND EXPERIMENTAL ATHEROSCLEROSIS AND VASCULAR IMAGING IN PSITTACIFORMES A Dissertation Submitted to the Graduate Faculty of the Louisiana State University and Agricultural and Mechanical College in partial fulfillment of the requirements for the degree of Doctor of Philosophy in The Department of Veterinary Clinical Sciences by Hugues Beaufrère Dr.Med.Vet., University of Lyon, France, 2006 Diplomate ABVP – Avian Practice, 2012 Diplomate ECZM (Avian), 2012 May 2013 A Mélanie, qui élève mon cœur. ii ACKNOWLEDGEMENTS First and foremost, I would like to express my thanks to my mentors, Drs. Thomas Tully and Javier Nevarez. Their help, guidance, and trust were instrumental in the completion of my program and these research projects. They promoted unique opportunities at LSU that were far beyond what was just required to succeed in this program. My time within the Zoological Medicine Service will always be remembered as a pivotal point in all my accomplishments. I would like to express my deepest gratitude to Dr. Tully who believed in me from early on when I was just a veterinary student. Dr. Tully consistently demonstrated that science was about sharing and collaborating and this, in combination with his continuous support and mentorship, shaped my vision of learning and teaching avian medicine. I would like to recognize Dr. Nevarez for his constant assistance and for putting me back on the right track when I was “slightly” diverging from initial plans. He managed somehow to insufflate the rigor and meticulousness necessary to all scientific work into my innate sense of chaos. My sincere appreciations also go to the other members of my committee. Dr. Romain Pariaut who was always ready for a new avian cardiologic adventure and whom I consider not only as the transesophageal ultrasound probe bearer, but also as a friend. We are grateful to Dr. Nobuko Wakamatsu who assisted in histopathological interpretation and who was always available when needed. It was a pleasure to work with her. I would like to thank Dr. Heatley for sharing research resources and findings with me and participating in this committee. I would also like to acknowledge the help and teaching of Dr. Brian Marx who contributed to anchoring in me a strong interest in applied biostatistics, a valuable skill that served me well during my studies even if I could never be confident to be right 95% of the time. Furthermore, I would like to acknowledge the help of all my other co-authors, Dr. Daniel Rodriguez for having performed close to 1700 imaging measurements for my studies, Dr. Lorrie Gaschen for her trust in my CT project and for her assistance, Dr. Drury Reavill for having sent me a countless number of pathology slides in a timely fashion, Dr. Michael Garner for having received me in his house and given me access to his histopathology slides database, Dr. Carolyn Cray for having provided clinical pathology support, Dr. Susan Clubb for having supplied the Quaker parrots, Dr. Kali Holder for her assistance in the atherosclerosis classification study, and Dr. Mélanie Ammersbach, my wife, who managed somehow to squeeze her name in one of my PhD publications and actually gave me the idea for my epidemiological study. In addition, I would like to thank our funding sources without which none of this research would have been possible. The Department of Veterinary Clinical Sciences funded the largest part of these studies and we are thankful to all its members for supporting psittacine cardiovascular research and graduate students at LSU. We are also extremely grateful to the Kaytee Avian Foundation, Mr. Rich Bonkowski, and Dr. Randal Brue for their invaluable help with the dietary aspect of our atherosclerosis model study and for supporting the LSU Hispaniolan Amazon parrot colony. We recognize the financial support of the South Alabama Bird Club that provided funds necessary to the completion of our CT study. Finally, I would like to thank my family and particularly my parents who supported me unconditionally throughout my veterinary studies and post-graduate training. Without them, I would be like a bird without wings. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ...................................................................................................... iii ABSTRACT ............................................................................................................................. vii INTRODUCTION ......................................................................................................................1 LITERATURE REVIEW............................................................................................................3 I. Avian cardiology ..................................................................................................................3 A. Anatomy and physiology of the avian cardiovascular system ........................................3 B. Diagnostic techniques .....................................................................................................7 C. Cardiovascular diseases of birds (other than atherosclerosis) ......................................22 II. Atherosclerosis in mammals .............................................................................................38 A. Pathogenesis..................................................................................................................38 B. Atherosclerotic lesions ..................................................................................................44 C. Risk factors for atherosclerotic vascular disease ..........................................................47 D. Diagnostic techniques ...................................................................................................51 E. Medical management and treatment .............................................................................53 F. Mammal models of atherosclerosis ...............................................................................56 III. Avian atherosclerosis .......................................................................................................60 A. Peculiarities of avian lipoprotein metabolism ..............................................................60 B. Avian models of atherosclerosis ...................................................................................61 C. Psittacine atherosclerosis ..............................................................................................63 D. Atherosclerosis in non-domestic avian species ............................................................73 CHAPTER I: CHARACTERIZATION AND CLASSIFICATION OF PSITTACINE ATHEROSCLEROTIC LESIONS BY HISTOPATHOLOGY, DIGITAL IMAGE ANALYSIS, TRANSMISSION AND SCANNING ELECTRON MICROSCOPY ............76 I. Introduction ........................................................................................................................76 II. Materials and methods ......................................................................................................78 A. Sample collection ..........................................................................................................78 B. Histopathology ..............................................................................................................78 C. Digital image analysis ...................................................................................................79 D. Transmission and scanning electron microscopy .........................................................80 E. Classification of atherosclerotic lesions ........................................................................81 F. Statistical analysis .........................................................................................................81 III. Results .............................................................................................................................81 A. The normal intima and arterial wall ..............................................................................85 B. Type I lesions ................................................................................................................86 C. Type II lesions ...............................................................................................................86 D. Type III lesions .............................................................................................................87
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