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Characterising Adaptational Dysfunction in Age-Related Macular Degeneration

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Characterising Adaptational Dysfunction in Age-Related Macular Degeneration Characterising adaptational dysfunction in age-related macular degeneration A thesis submitted to Cardiff University for the degree of Doctor of Philosophy By Allannah Jayne Gaffney School of Optometry and Vision Sciences Cardiff University August 2012 Supervised by Dr Alison Binns and Dr Tom Margrain Summary Age-related macular degeneration (AMD) is the leading cause of visual impairment in the developed world (Resnikoff et al., 2004). The prevalence of this disease will continue to increase over the coming decades as the average age of the global population rises (United Nations, 2009). There is consequently an urgent need to develop tests that are sensitive to early visual dysfunction, in order to identify individuals that have a high risk of developing AMD, to identify patients that would benefit from treatment, to assess the outcomes of that treatment and to evaluate emerging treatment strategies. An emerging body of evidence suggests that dark adaptation is a sensitive biomarker for early AMD. Cone dark adaptation is of particular interest to clinicians, as it can identify patients with early AMD in a relatively short recording period. Consequently, this thesis aimed to optimise psychophysical and electrophysiological techniques for the assessment of cone dark adaptation in early AMD, in order to maximise its diagnostic potential. A range of psychophysical methods were shown to be capable of monitoring the rapid changes in threshold that occur during cone dark adaptation. An optimal psychophysical protocol for the assessment of cone dark adaptation in early AMD was developed based on the results of a systematic evaluation of the effect of stimulus parameters and pre-adapting light intensity on the diagnostic potential of cone dark adaptation in early AMD. When compared to the focal cone ERG photostress test, both techniques were shown to be similarly diagnostic for early AMD. In addition, the time constant of cone recovery was shown to be significantly correlated with age, hence the sensitivity and specificity of cone dark adaptation as a biomarker for early macular disease may be further improved by considering these age-related changes. In conclusion, this thesis has confirmed that cone dark adaptation is a sensitive functional biomarker for early AMD. However, as cross-sectional studies are unable to determine the true diagnostic potential of a biomarker, longitudinal investigations are needed to explore the long-term potential of cone dark adaptation and other visual functions as biomarkers for early AMD. i Acknowledgements Having spent a considerable amount of time quite literally ‘in the dark’ during the course of this thesis, I must express my gratitude to those individuals who have helped me along the way. Firstly, my sincere thanks to my two inspirational supervisors, Dr Alison Binns and Dr Tom Margrain, for all of their advice and encouragement throughout the last few years. I feel extremely lucky to have worked as part of their team and I hope I can continue to do so for some time to come! Many thanks to all the dedicated participants that spent hours in darkness in order to generate the data presented in this thesis. In hindsight I can’t quite believe all that I put them through, yet without exception, they greeted everything thrown at them with excellent humour and certainly made my job much more enjoyable! Thank you to the residents of room 2.10, past and present, for their friendship and support - I’m quite sure that the distractions that come with working in a communal office play an integral role in completing a thesis! Thank you also to Sue, Leanne and the many other supportive staff at Maindy Road for making the Optometry department such a pleasant working environment. A big thank you to the Gaffney family for the constant encouragement they have given me over the years and for conscientiously listening to intricate explanations of the many ‘interesting’ projects that I have pursued! Last, but by no means least, thank you to Amar for making me smile each day – exactly as I asked. ii Contents Summary i Acknowledgements ii Contents iii List of Figures x List of Tables xiv List of abbreviations xvi Chapter 1. Introduction 1 1.1. The healthy retina ……………………………………………………… 1 1.1.1. Healthy macular anatomy ……………………………………… 3 1.1.2. Bruch’s membrane ……………………………………………… 3 1.1.3. The retinal pigment epithelium (RPE) …………………………… 4 1.1.4. Photoreceptor cells ………………………………….................... 5 1.1.5. Bipolar cells ……………………………………………………… 7 1.1.6. Horizontal cells …………………………………………………… 8 1.1.7. Müller cells ……………………………………………………… 8 1.1.8. Amacrine cells …………………………………………………… 9 1.1.9. Retinal ganglion cells (RGCs) …………………………………… 9 1.1.10. The visual pathway ……………………………………………… 10 1.2. Age-related macular degeneration (AMD) ……………………………… 11 1.2.1. Incidence and prevalence of AMD ……………………………… 11 1.2.2. Clinical features of AMD ……………………………………… 12 1.2.2.1. Drusen ……………………………………………… 12 1.2.2.2. Pigmentary abnormalities ……………………………… 13 1.2.2.3. Geographic atrophy (GA) ……………………………… 13 1.2.2.4. Neovascular AMD (nAMD) ……………………………… 14 1.2.2.5. Pigment epithelial detachment (PED) ……………… 14 1.2.3. Clinical classification of AMD ……………………………… 14 1.2.4. Risk factors for AMD ……………………………………… 16 iii 1.2.4.1. Smoking ……………………………………………… 16 1.2.4.2. Genetics ……………………………………………… 17 1.2.4.3. Race ……………………………………………………. 17 1.2.4.4. General health ……………………………………… 17 1.2.4.5. Diet ……………………………………………………. 18 1.2.4.6. Sunlight ……………………………………………… 19 1.2.5. Pathogenesis of AMD ……………………………………… 19 1.2.5.1. Oxidative stress ……………………………………… 19 1.2.5.2. Lipofuscin formation ……………………………… 20 1.2.5.3. Chronic inflammation and the immune response ……… 21 1.2.5.4. Hypoxia and choroidal vascular changes ……………… 22 1.2.6. Clinical investigation of AMD ……………………………… 23 1.2.6.1. Fundus photography ……………………………… 23 1.2.6.2. Fundus angiography (FA) ……………………………… 24 1.2.6.3. Fundus autofluorescence (FAF) ……………………… 24 1.2.6.4. Optical coherence tomography (OCT) ……………… 24 1.2.6.5. Visual acuity ……………………………………… 25 1.2.6.6. Visual field testing ........................……………………… 26 1.2.6.7. Contrast sensitivity ……………………………………… 27 1.2.6.8. Temporal sensitivity ……………………………………… 27 1.2.6.9. Colour vision ……………………………………… 27 1.2.6.10. Dark adaptation ……………………………………… 28 1.2.7. Prevention and treatment ……………………………………… 28 1.2.7.1. Focal laser photocoagulation ……………………… 28 1.2.7.2. Verteporfin photodynamic therapy (PDT) ……………… 29 1.2.7.3. Anti-VEGF drugs ……………………………………… 29 1.2.7.4. Management of dry AMD ……………………………… 31 1.2.7.5. Novel therapies ……………………………………… 31 1.3. Visual adaptation ……………………………………………………… 32 1.3.1. Dark adaptation ……………………………………………… 32 1.3.2. Physiology of dark adaptation: the retinoid cycle ……………… 34 1.3.3. The Müller cell hypothesis: An alternative pathway for photopigment regeneration ……………………………………… 36 1.3.4. The retinoid cycle and visual threshold during dark adaptation ….. 37 iv 1.3.4.1. The photochemical hypothesis ……………………… 37 1.3.4.2. The equivalent background hypothesis ……………… 38 1.3.5. Adaptational dysfunction ……………………………………… 40 1.3.5.1. Dark adaptation and age ……………………………… 40 1.3.5.2. Dark adaptation and retinal disease ……………… 41 1.3.5.3. Dark adaptation in AMD ……………………………… 42 1.3.5.4. Photostress recovery in AMD ……………………… 44 1.4. Visual psychophysics ……………………………………………………… 44 1.4.1. Classical psychophysical methods ……………………………… 45 1.4.1.1. The method of constant stimuli ……………………… 46 1.4.1.2. The method of limits ……………………………… 46 1.4.1.3. The method of adjustment ……………………… 46 1.4.1.4. Disadvantages of classical psychophysical methods …… 47 1.4.2. Adaptive psychophysical methods ……………………………… 47 1.4.2.1. The staircase procedure ……………………………… 48 1.4.2.2. Parameter estimation by sequential testing (PEST) ……. 48 1.4.2.3. Maximum-likelihood procedures ……………………… 48 1.4.3. Forced-choice psychophysical methods ……………………… 49 1.4.3.1. Forced-choice methods ……………………………… 50 1.4.3.2. Yes-no methods ……………………………………… 50 1.4.4. Psychophysical assessment of dark adaptation ……………… 51 1.5. The electroretinogram (ERG) ……………………………………………… 52 1.5.1. The transient (flash) ERG ……………………………………… 52 1.5.1.1. Early receptor potential (ERP) ……………………… 53 1.5.1.2. a-wave ……………………………………………… 53 1.5.1.3. b-wave and oscillatory potentials ……………………… 54 1.5.1.4. Photopic negative response (PhNR) ……………… 55 1.5.1.5. Scotopic threshold response (STR) ……………… 55 1.5.1.6. c-wave ……………………………………………… 55 1.5.1.7. d-wave ……………………………………………… 56 1.5.2. The steady state (flicker) ERG ……………………………… 56 1.5.3. The focal ERG ……………………………………………… 57 1.5.4. The multifocal ERG (mfERG) ……………………………… 57 1.5.5. The pattern ERG (PERG) ……………………………………… 58 v 1.5.6. Recording the ERG ……………………………………………… 59 1.5.6.1. Electrodes ……………………………………………… 59 1.5.6.2. Electrical noise and noise reduction ……………… 60 1.5.6. The ERG in AMD ……………………………………………… 62 1.5.7. Assessment of dark adaptation using the ERG and related techniques 64 1.6. Overview and aims ……………………………………………………… 65 Chapter 2. A comparison of psychophysical methods of 69 monitoring cone dark adaptation 2.1. The repeatability of the Goldmann-Weekers adaptometer for monitoring cone dark adaptation .…………………………………………………………… 70 2.1.1. Introduction ……………………………………………………… 70 2.1.2. Aims ……………………………………………………………… 71 2.1.3. Methods ……………………………………………………… 71 2.1.4. Results ……………………………………………………… 74 2.1.5. Discussion ……………………………………………………… 77 2.2. A comparison of four psychophysical methods for monitoring cone dark adaptation ……………………………………………………………… 78 2.2.1. Introduction ……………………………………………………… 78
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