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Monitoring of Diabetic Retinopathy and Changes in Related Biomarkers After Bariatric Surgery in Patients with Type 2 Diabetes

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Monitoring of Diabetic Retinopathy and Changes in Related Biomarkers After Bariatric Surgery in Patients with Type 2 Diabetes UNIVERSITY OF COPENHAGEN FACULTY OF HEALTH AND MEDICAL SCIENCES PhD Thesis Troels Brynskov, MD Monitoring of Diabetic Retinopathy and Changes in Related Biomarkers after Bariatric Surgery in Patients with Type 2 Diabetes FACULTY OF HEALTH AND MEDICAL SCIENCES UNIVERSITY OF COPENHAGEN Monitoring of Diabetic Retinopathy and Changes in Related Biomarkers after Bariatric Surgery in Patients with Type 2 Diabetes PhD thesis Troels Brynskov, MD This thesis has been submitted to the Graduate School at the Faculty of Health and Medical Sciences, University of Copenhagen 1 PhD thesis “Monitoring of Diabetic Retinopathy and Changes in Related Biomarkers after Bariatric Surgery in Patients with Type 2 Diabetes” Troels Brynskov, MD Department of Ophthalmology, Zealand University Hospital Roskilde, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark [email protected] +45 50 50 78 89 Submission date: 16 January 2016 Academic advisors Torben Lykke Sørensen, MD, DMSci, Professor Department of Ophthalmology, Zealand University Hospital Roskilde, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark Caroline Schmidt Laugesen, MD Department of Ophthalmology, Zealand University Hospital Roskilde, Denmark Assessment committee Henrik Lund Andersen, MD, DMSci, Professor (Chair) Department of Ophthalmology, Copenhagen University Hospital Glostrup, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark Jakob Grauslund MD, PhD, Professor Department of Ophthalmology, Odense University Hospital, Denmark University of Southern Denmark Stela Vujosevic, MD, PhD, Assistant Professor Department of Ophthalmology, University of Padova, Italy Cover art: Own montage of a) Iris by Nevermind04/reddit.com and b) fundus image of patient #4. 2 Table of contents PREFACE 5 ABBREVIATIONS AND ACRONYMS 7 LIST OF PUBLICATIONS 8 INTRODUCTION 9 BACKGROUND 10 TYPE 2 DIABETES 10 BARIATRIC SURGERY 13 DIABETIC RETINOPATHY 14 THE IGF AXIS 20 BARIATRIC SURGERY AND END-ORGAN COMPLICATIONS 20 OBJECTIVES 22 METHODS 23 STUDY DESIGN 23 PATIENTS 23 EXAMINATIONS AND GRADING 24 STATISTICAL ANALYSIS 31 RESULTS 32 RECRUITMENT 32 PREOPERATIVE CHARACTERISTICS 33 CHANGES IN NON-OCULAR OUTCOMES 33 CHANGES IN DIABETIC RETINOPATHY 34 CLINICAL CHANGES IN MACULOPATHY 38 EXPLORATORY ANALYSIS OF SUBCLINICAL CHANGES IN RETINAL THICKNESS 39 CHANGES IN VISUAL ACUITY 42 CHANGES IN VESSEL CALIBERS 42 THE IGF AXIS 43 3 DISCUSSION 48 DIABETIC RETINOPATHY 48 CHANGES IN VISUAL ACUITY 51 SUBCLINICAL OCULAR CHANGES 51 CHANGES IN NON-OCULAR OUTCOMES 53 VALIDITY 54 LIMITATIONS 56 PERSPECTIVES 58 CONCLUSIONS 60 SUMMARY 61 DANSK RESUMÉ (SUMMARY IN DANISH) 63 REFERENCES 65 APPENDICES PAPER I PAPER II PAPER III 4 Preface I completed the studies within this PhD thesis during my employment at the Department of Ophthalmology, Zealand University Hospital Roskilde 2012–2015. Within this period I have had the fortunate experience of how the field of ophthalmology is undergoing an exciting transformation, as new treatments are emerging for which no or little treatment were previously available. Specifically, the introduction of intravitreal anti- vascular endothelial growth factor for wet age-related macular degeneration, retinal vein occlusion and diabetic retinopathy has revolutionized the prognosis for patients with these diseases. Stem cell therapies and gene therapy are also taking off and multitudes of new imaging modalities are rapidly transforming the field of ophthalmology – it is a very exciting time to be an ophthalmologist! So many people made this project possible and I am indebted to everyone who was involved from the very beginning to the end. First and foremost, I wish to thank my supervisors Professor Torben Lykke Sørensen and Caroline Schmidt Laugesen from the bottom of my heart! Thank you for trusting me with the project and for welcoming me at the department in Roskilde. Torben, you have been an enormous inspiration, both professionally and personally. Thank you for many great moments shared during these past years and for helping me to see the forest when all I could see was trees and lumber. You have been the greatest possible mentor with an always-open door. Caroline, you are my role model! You have taught me a lot about being an ophthalmologist – every day I strive to become just a little bit more like you. Also a big thanks to Henrik Kemp who always makes things happen and all staff members at the Department of Ophthalmology in Roskilde, who were always open and supportive. It has been an enormous pleasure to be a part of the growing research unit at the department of ophthalmology in Roskilde. In particular, I would like to thank my fellow PhD-colleagues Amardeep Singh, Mads Falk, Yousif Subhi and Marie Krogh Nielsen, for all the great times and for all the advice, help, moral support and assistance along the way. In particular Yousif who proofread the manuscript for this thesis. Ane Maria Bang Korsholm also deserves praise for laying some of the initial foundation for this project. Throughout the project, I have had the fortune to be welcomed with a smile and positive attitude, wherever I came. I had the pleasure to collaborate with Andrea Karen Floyd and Annette Lykke Svenningsen from the Department of Bariatric Surgery in Køge. Without their support, there would have been no project at all! The level of recruitment was extraordinary thanks to the efforts of them and everyone else at the Department of Bariatric Surgery in Køge. At the Department of Biochemistry in Roskilde, I could always count on the help and assistance of Marianne Boslev and Birthe Nyberg and their staff. Professor Jan Frystyk provided 5 invaluable expertise with blood samples and provided great feedback for Paper III. His staff from the Medical Research Laboratory at Aarhus Universitetshospital, especially Nils Erik Magnussen and Susanne Sørensen also provided their excellent and attentive assistance with the assays. Malin Lundberg Rasmussen from the Department of Ophthalmology at Odense Universitetshospital was a tremendous help in establishing the image grading procedures. Professor Michael Larsen, Oliver Niels Klefter, Hajer Ahmad Al-Abaiji and Sermed Zyad Khalil Al-Hamdani of the Department of Ophthalmology at Glostrup Hospital generously assisted me with becoming acquainted with the software for the measurement of retinal vessels. The staff at the Department of Biostatistics at Copenhagen University was always very helpful whenever I needed assistance, especially Julie Lyng Forman. Luise Jessen Lundorf provided thoughts and comments for the manuscript for this thesis were sharp as a razor. Of course. Thank you very much. The generous support of Fight for Sight Denmark (Øjenforeningen), The Bagenkop Nielsen Myopia foundation and the Research Foundation of the Zealand Region made this project economically feasible. I would also like to thank all the patients who went through all the hassle of scheduling, transportation and tedious examinations in order to make this project happen. This thesis is not mine — it is yours! Last, but certainly not least: my fantastic backing crew. Above all, my gorgeous wife-to-be Lena and our two energetic dynamos Viggo and Ludvig. And my parents Morten and Tove, and the rest of my family, in-laws and friends. I am so fortunate to have you in my life, I love you very much, and none of this would have been possible, or worthwhile, without you. Copenhagen, January 2016 Troels Brynskov 6 Abbreviations and acronyms Abbreviations and acronyms that appear in this thesis except for standard abbreviations in the Diabetologia style guide (http://www.diabetologia-journal.org/webpages/styleguide/abbreviations.html): ACCORD Action to Control Cardiovascular Risk in Diabetes trial ACR Albumin Creatinine Ratio CRAE Central Retinal Artery Equivalent CRVE Central Retinal Vein Equivalent DCCT Diabetes Control and Complications Trial ETDRS Early Treatment Diabetic Retinopathy Study trial GCL Ganglion Cell Layer GH Growth Hormone GLP-1 Glucagon-Like Peptide-1 IGF Insulin-like Growth Factor IGFBP Insulin-like Growth Factor Binding Protein INL Inner Nuclear Layer IPL Inner Plexiform Layer IRMA Intraretinal Microvascular Abnormality OCT Optical Coherence Tomography ONL Outer Nuclear Layer OS Outer Segment of photoreceptors RNFL Retinal Nerve Fiber Layer RPE Retinal Pigment Epithelium SOS Swedish Obesity Subjects STAMPEDE Surgical Therapy and Medications Potentially Eradicate Diabetes Efficiently VEGF Vascular Endothelial Growth Factor WESDR Wisconsin Epidemiologic Study of Diabetic Retinopathy UKPDS United Kingdom Prospective Diabetes Study 7 List of publications Paper I: Brynskov T, Laugesen CS, Svenningsen AL, Floyd AK, Sørensen TL. Monitoring of Diabetic Retinopathy in relation to Bariatric Surgery: a Prospective Observational Study. Obesity Surgery, 2016;26:1279-1286. Paper II: Brynskov T, Laugesen CS, Svenningsen AL, Floyd AK, Sørensen TL. Thickening of inner retinal layers in the parafovea after bariatric surgery in patients with type 2 diabetes. Acta Ophthalmologica, 2016. Epub ahead of print. Paper III: Brynskov T, Laugesen CS, Floyd AK, Frystyk J, Sørensen TL. The relationship between diabetic retinopathy and the IGF-axis before and after gastric bypass surgery. Obesity Surgery, 2016. Epub ahead of print. 8 Introduction Sight is our most precious sense. To prevent sight loss is even more important than to treat sight-threatening diseases when they occur. Diabetic retinopathy is a common disease but predicting progression
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