Practical Handbook of Fluorescein Angiography: Posterior Pole and Retinal Periphery Bruno Lumbroso, Marco Rispoli
INDEX
Note: Page numbers in bold or italic refer to tables, box or figures respectively.
A
Adenovirus 38
Albescent punctate retinopathy 27
Albipunctate dystrophy 86
Angiitis 112
Angiography, role of 131
Angioid streaks 119
Antistreptolysin O 38
Antivascular endothelial growth factor 67, 134
Arterial capillaries 66
Arterial filling 9
Arterial phase 5
Arteriovenous phase 5
Artery occlusion 51, 91
Artifacts 20
Artificial intelligence 143
Astrocytic hamartomas 8
Atheroma plaque 51
Autofluorescence 8, 61
Avascular retina, edge of 119
B
Behçet's disease 38
Best's disease 51
Bipolar cell bodies 3
Blind spot 109
Blindness 86
Blood disorder 54, 90
Blood-ocular barrier 13
Blood-retina barrier 58, 58
internal 32, 58
outer 58
Branch artery occlusion 94, 95
Branch vein occlusion 50, 9294
ischemic 54
Brucellosis 38
Bruch's membrane 3, 40, 41, 44, 77, 97, 106
rupture of 32
B-scan analyses 20
Bull's eye 27, 86, 87
dystrophy 86
lesion 86
macular dystrophy 86
maculopathy 86, 87, 87
C
Capillary dilatations 66
Capillary dropout, nonperfused areas of 21
Capillary phase 5
Cardiac and cardiovascular complications, severe 19
Carotid diseases, internal 96
Carotid stenosis 57
Cat scratch disease 38
Cell apoptosis 97
Central retina
arterial occlusion 91
artery 91
normal fluorescein angiography of 5
Central retinal vein 57
occlusion 89, 116
Central retinitis pigmentosa 84
Central serous chorioretinopathy 27, 32, 3336, 97, 100, 101
differential diagnosis of 38
fluorescein angiography 99
Central vein ischemic occlusion 91
Chloroquine 84, 86, 87
Choriocapillaris 5, 27, 40, 58, 75, 79
blood flow alterations 79
Chorioretinal inflammatory localizations 109
Chorioretinal scars 44
Chorioretinitis 27
Choroid 4, 6, 11, 17, 49, 53, 57, 58
areolar atrophy of 53
circulation 11
abnormalities of 13
layer 85
leakage 33
melanoma of 106
normal fluorescein angiography of 11
pooling in 40
vascular supply 4
veins of 4
vessels
main 11
small 11
Choroidal blood flow 134
Choroidal fluorescence 27
normal 83
Choroidal granular fluorescence 30
Choroidal hemangioma 131, 132, 133
Choroidal melanoma 45, 107, 131, 132, 134136
treatment 134
Choroidal metastases 136, 137
retinography 137
Choroidal neovascularization 19, 20, 22
Choroidal nevus 106, 132, 133, 134
peripheral 134
Choroidal osteoma 136, 138
Choroidal phase 5, 6, 9, 9
Choroidal thickness 98
Choroidal tissue 98
Choroidal tumors 108
Choroidal vessels 137
wide 11
Choroideremia 53
Choroiditis 144
active 111
granuloma 51
Choroidopathy, exudative 32, 33
Choroid-vortex veins 4
Chronic central serous chorioretinopathy 29, 97, 98, 100
Ciliary artery 5, 94
posterior 3
short posterior 5
Ciliary vessels, posterior 58
Coat's disease 22, 34, 120
Colloid bodies 75
Concentric annular dystrophy, benign 87
Concentric retinitis pigmentosa 117
Cone-rod dystrophy 86
Coxsackie virus A10 38
Cryoglobulinemia 56, 73
Cystoid macular edema 34, 42, 43, 71, 72, 83, 104
advanced 71
cells 80
causes of 48
differential diagnosis of 48
edema 104
Cytomegalovirus 38
D
Dark choroidal mass, diagnosis of 108
Dark subepithelial hemorrhages 77
Dark lesion in 105, 106
diagnosis of 105
early phase 108
late phase 108
Deep choroidal hemorrhage 37
subretinal 105
Deep retinal
capillaries 20
layers 66
Diabetes mellitus
type 1 123
type 2 123
Diabetic background retinopathy 66
Diabetic maculopathy 71, 72
Diabetic microangiopathy 46
Diabetic retinopathy 15, 16, 21, 51, 55, 56, 56, 65, 6672, 73, 123
classification of 123, 123
early stages of 68
nonproliferative 21, 65, 67, 123
mild 123, 124, 125
moderate 123, 126
severe 70
proliferative 65, 7274, 123
mild 127
study, early treatment 123
Diffuse macular edema, causes of 48
Diskiform macular degeneration 82
Drepanocytosis 55
E
Eales’ disease 32, 51, 56
Early venous phase 5
Edematous branch vein occlusion 93
Edematous forms 89
Ellipsoid 98
Endothelial cells 65
Epiretinal membrane 72, 103
causes of 103
Epithelial alterations
atrophic 131
dystrophic 131
Epithelial hypertrophy 105
Epitheliopathy, chronic 29, 32, 98
Epstein–Barr virus 38
Ethambutol 84
Exudative hemorrhagic chorioretinopathy, peripheral 132, 137, 138
Eye
fundus of 6
membranes of 61
pressure 61
F
Familial adenomatous polyposis 137
Familiar exudative vitreoretinopathy 119
Faster vascular filling 57
Fibroglial tissue 82
Fibrous diskiform scar 78
Fibrovascular tissue 79, 81
Filling
accelerated 57
defects 51, 52, 53, 5456
delayed 57, 57
Flu-like symptoms, mild 109, 110
Fluorangiography 125
Fluorescein 19
angiograms 62
angiographic lesions 69
assessment of 19
pooling 34, 39
Fluorescein angiography 3, 11, 13, 19, 20, 21, 22, 22, 27, 36, 39, 45, 58, 61, 62, 65, 70, 100, 105, 107, 108, 109, 115, 116, 120, 132, 143
abnormal 13
alterations 61
assessment 61
disadvantages of 19
future of 143, 144
phases 61
role of 13
syndromes, major 63
Fluorescence
abnormal transmission of 27
angiography 66
anomalous transmission of 2831
Focal and diffuse edema 71
Foveal avascular zone 21
Frosted branch vasculitis 109, 112
Fundus 11
autofluorescence 61, 85
examination 13
flavimaculatus 86
G
Ganglion cell
complex 67
layer 3
Gardner syndrome 137
General circulatory disorders 57
Geographic atrophy 32
Glaucoma 90, 91
vascular 65, 93
Gravitational epitheliopathy 97, 98, 99, 100
causes of 101
fluorescein angiography 97
Griseofulvin 84
H
Haller layer 4, 11
Harada's disease 32
Hard exudates 70
Hemorrhage 49, 58, 70, 73
causes of
deep 50
preretinal 49
superficial 49
choroidal 49, 50
deep 50
infiltrate retina 83
intratumor 106
preretinal 50, 73
retinal 125
subepithelial 78, 83
subretinal 50, 75, 77, 78, 83, 139
superficial 50
vitreous 49, 73, 123
Hereditary macular
atrophies 84
dystrophies 84, 86
Hereditary maculopathy 86
Herpes simplex 38
Herpes zoster-varicella 38
Hutchinson–Siegrist
syndrome 32
traumatic retinopathy 31
Hydroxychloroquine 86, 87
Hyperfluorescence 9, 13, 27, 32, 39, 44, 61
abnormal 13, 27, 27
granular microdots 83
pseudocystic cavities 71
spot 36
type of abnormal 27
Hyperplasia 52
Hyperreflective mass 107
Hypofluorescence 49, 53, 61
elements 13
I
Idiopathic disorder 109
Idiopathic polypoidal
chorioretinopathy 84
vasculopathy 79, 85
Indocyanine angiography, assessment of 19
Indocyanine green angiography 22, 61, 131
Indomethacin 84
Infection 90
Inferior retinal
detachment 133
periphery 120
Inflammatory disorders 109, 110112
Intraretinal cavities 39
Intraretinal microvascular abnormalities 65, 67, 125
Intraretinal neovascularization 67
Intravitreal antiangiogenic treatments 65, 73
Inverse pigmentary dystrophy 84
Iris 89
Ischemia, level of 65
Ischemic capillaropathy 90
Ischemic capillary lesions 66
Ischemic forms 89
Ischemic maculopathy 72
Ischemic optic disk disorders 58
Ischemic retinal areas 65
Ischemic vascular alterations leading to proliferative retinopathy 71
Ischemic vein occlusion 94
L
Lamina cribrosa 9
Laminar flow 7
Laser
photocoagulation 65
treatment 120
Laurence–Moon–Bardet–Biedl syndrome 87
Leopard spot 136
Less frequent causes of macular edema 90
Leukemia 56, 73
Lipofuscin 134
presence of 8
Lobules 4
Lupus erythematosus 52
Lyme disease 38
M
Macroaneurysms 32
causes of 48
Macula 3
normal 69
Macular area 3
Macular atrophy 84
acquired 84
Macular degeneration 32, 75, 7578, 79, 7987
age-related 21, 28, 32, 49, 75, 78, 79, 81
senile 75
treatment of age-related 78
Macular disease, varieties of 21
Macular dystrophy 79, 84
acquired 84
Macular edema
diabetic 65, 123
cystoid 72
post-treatment 125
Macular pucker 104
Measles 38
Melanoma 108
Membrane
epiretinal 103
preretinal 103
Metamorphopsia 123
Microaneurysm 20, 32, 67, 125
differential diagnosis of 48
Mimic melanoma 139
Moschowitz disease 54
Myeloma, multiple 56, 73
Myopia 53
N
Neovascular proliferation 65
Neovascular tissue 19
Neovascularization 22, 32
Nerve fiber layer, dissociation of 104
Nonperfused arteries 94
Nonperfusion peripheral retina 55
Nonproliferative retinopathy 65
developmental stage of 72
severe 123
Normal fluorescein angiography 5
Normal fluorescence, mask effect of 49
Nuclear layer, outer 11
O
Occult neovessels 78
Ocular frequent causes of venous occlusion 90
Ocular fundus 131
Ocular high pressure 96
Ocular oncology 131
Ophthalmoscopic examination 131
Optic disk 4, 9, 73, 106, 111
filling 9
normal 9
fluorescein angiogram of 9
Optic nerve 57, 58
Optical coherence tomography 65, 105
angiography 1921, 33, 79, 90, 97, 143
Optical coherence tomography angiography 19, 20, 20
advantages of 20
disadvantages of 20
Optical-ciliary anastomoses 89
Ora serrata 3
Outer retinal
layers 71
tubulation 83
P
Pachychoroid disorders, part of 32
Pachychoroid neovasculopathy 97, 98
Pachychoroid spectrum 84, 97
Papilla 6, 11, 73
drusen of 8
Papillary neovascularization, causes of 73
Papillary pseudoedema 8
Papillitis, mild 111
Parasitosis 108
Pathological fluorescein angiography 13
analytical study 25
synthesis 59
Pattern dystrophy fundus autofluorescence 86
Perifoveal arcades 20
Perilesional epithelial dystrophy 131
Perimacular capillary network alterations 69
Peripheral retina 3, 116
tumor 132
Phenothiazine 84
Pigment 49
hyperplasia 50
scar 105
Pigment epithelium 4, 44, 58, 75, 82, 92, 97
detachment 41, 97
causes of 39
hyperplasia of 50
hypertrophy 105, 105
tears 78
Placoid epitheliopathy 30
Plasma-erythrocyte separation 132
Plexiform layer
inner 3
outer 11, 67
Polypoid angiomatous formation 84
Polypoid choroidal vasculopathy 97
Polypoidal angiomas, cluster of 85
Pooling pigment epithelium detachment 40
Posterior pole 3
Preretinal neovascularization, causes of 73
Proliferative retinopathy 71, 72
early 123
Pseudofluorescence 7
Pseudomelanomas 137
Q
Quincke's edema 19
R
Radial capillary network 6
Radiation retinopathy 134, 136
Regional rare causes of venous occlusion 90
Regressive cystoid edema, causes of 48
Reticular dystrophy 84
Retina 4, 11, 17, 40, 44, 51, 53, 57, 58, 72, 77, 78, 85, 89, 94, 100, 105
abnormal 13
affected 94
arm to retina phase 5
avascular 120
causes of serous elevation of 38
central vein of 91
hemorrhagic detachments of 79
inner 95
laser treatment of 53
layers, internal 78, 92
levels of 49
normal 66
periphery 3
reconstruction, total 14, 15
retinal lesions causes of window defects 32
sensory 3
serous detachment of 82
staining 46
thickness 70
vessels of 73
Retinal anatomy 3
Retinal and papillary neovascularization, causes of 39
Retinal angiomas 32, 38
leakage and pooling in 33
Retinal angiomatous proliferations 78
Retinal arterial
occlusion, causes of 96
vessels 95
Retinal arterioles 66
Retinal artery 3, 5, 5, 6, 121
Retinal capillary 13
endothelium of 13
hemangioblastoma 132
superficial 20
Retinal cavernous hemangioma 132
Retinal central artery occlusion 94
Retinal circulation, abnormalities of 13
Retinal cysts 128
Retinal degeneration 53
Retinal detachment 35, 65
Retinal disorders 62, 143, 144
Retinal drusen 40
Retinal edema 14, 67, 112
Retinal epitheliopathies 97
Retinal fluorescein angiography 65
Retinal fluorescence 11
Retinal folds, causing 103
Retinal hole 32
Retinal hypoperfusion 69
Retinal hypoxia 66
Retinal inner layers 103
disorganization of 67, 70
Retinal ischemia 90, 124, 136
causes of 56
extensive 39, 73
Retinal leakage 32, 33, 35, 36, 99
Retinal microaneurysms, causes of 44
Retinal microhemorrhages 124
Retinal necrosis, acute 118
Retinal neovascularization 20, 89, 119, 127
Retinal pathology
complex 69
superficial 104
Retinal periphery 3, 115, 115, 116, 119, 120, 123
fluorescein angiography of 113, 115, 116
Retinal photocoagulation, targeted 125
Retinal pigment epithelium 4, 11, 13, 105, 134
congenital hypertrophy of 137
serous detachment 34
Retinal scars, causes of 87
Retinal serous detachment 37
Retinal superficial angiomas 38
Retinal tissue 72
Retinal vascular
abnormalities 21
alterations
macroaneurysms, pooling in 41
pooling in 34, 42
changes 127
hamartoma 132
tumors 131
Retinal vasoproliferative tumors 132
Retinal vein 3
branch occlusion 91
Retinal vessel 116
leakage from newly formed 32
walls 44
Retinitis 32
chronic 32
pigmentosa 27, 118
traumatic 32
Retinopathy of prematurity, regressed 121
pathophysiology of 120
Retinoschisis, causes of 48
Retrobulbar treatments 62
Rosette appearance 83
Rubella 38
S
Sarcoidosis 117
Sattler layer 4
Sattler's middle vessel layer, level of 98
Sausage-shaped dilatation 70
Scars 111
Scattered multifocal choroiditis 109, 110
Sclera 4
Serous
chorioretinopathy, chronic 32
detachment 71, 72
epitheliopathy, chronic 32
Serpiginous epitheliopathy 27
Sickle cell
anemia 51, 56
retinopathy 13
Small retinal pigment epithelium elevation, differential diagnosis of 48
Solar retinopathy 32
Spongy retina 71
Stargardt disease 84, 86, 87
Steroids 134
Subretinal deposits, causes of 52, 53
Subretinal fluid 99, 106
Subretinal formation, differential diagnosis of 108
Subretinal neovascular membranes, causes of 39
Subretinal new vessels 33
Synthesis 61
procedure 62, 62
process and deduction 62
Synthetic evaluation 61
Systemic rare causes of venous occlusions 90
T
Tamoxifen 84, 86, 87
Telangiectasia, peripheral 118
Temporal arteries 5
Temporal periphery retinal hypoperfusion 121
Temporal retina, inferior 38
Thalassemia 51
Therapeutic intravitreal implants 62
Tissue
phase 5, 6
late 8
staining 40
Toxic lesions 27, 32
Toxoplasmosis 38
Traction edema 72
Tractional retinal detachment 123
Transitory screen 51
Triangular syndromes 4
Tuberculosis 38
Tumor
mass 107
vascular 132
U
Ultra-widefield device 16
Ultra-widefield fluorangiography 127, 128, 132
Uveitis 112, 144
V
Varicella zoster virus 118
Vascular filling defects 51, 53, 57
Vascular hyperfluorescence 39
Vascular intraretinal abnormalities 70
Vascular malformations 53
Vascular occlusion 89, 89, 9095
Vascular retinal diseases 21
Vasculitis 32, 109, 112
causes of leakage lesions 38
leakage in 33, 37
Vasoproliferative tumor 139
Venous branch occlusion 46, 91
Venous laminar flow 6
Venous occlusion 51, 89, 103
causes of 90
lesions 33
Venous phase 6
early 7
late 5, 6, 7
Vessel wall staining 46
Vision 86
loss of 134
Visual field 13
Visual loss 112
severe 73
Vitreitis 117
Vitreomacular traction 104
Vitreoretinal interface syndrome 103, 103, 104
Vitreoretinal surgery 134
Vitreous 73
surgery 123
Vitritis, posterior 110
Vogt–Koyanagi–Harada disease 32
von Hippel disease 34, 42
W
Waldenstrom disease 56, 73
White dot syndromes 109, 111
Widefield angiography 131
Widefield fluorescein angiography devices 13
Widefield imaging devices 132
Window defect 27, 28, 30
causes of 32
X
Xanthophyllic pigment, density of 3
×
Chapter Notes

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1Interpreting a normal and pathological fluorescein angiography
Retinal anatomy and fluorescein angiography
Normal fluorescein angiography of the central retina
Normal fluorescein angiogram of the optic disk
Normal fluorescein angiography of the choroid
Interpreting a pathological fluorescein angiography2

Retinal anatomy and fluorescein angiographyChapter 1

 
INTRODUCTION
The analytical study of retinal anatomy in relation to fluorescence angiography requires the retina to be subdivided into the posterior pole that lies inside the vascular arcades, and the peripheral retina that is the area around the posterior pole and the optic disk. The peripheral retina is further divided into mid-periphery, far-periphery, and extreme periphery (ora serrata): It is also subdivided in nasal periphery and upper and lower temporal periphery.
 
POSTERIOR POLE
The longer horizontal axis of the oval-shaped posterior pole measures 8–10 mm (30–35°). Fluorescein angiography with a 45° angle allows for a single frame picture to be taken of the posterior pole, the optic disk, and part of the vascular arcades. Modern devices allow wide-angle angiography.
 
MACULAR AREA
The macula, with a thickness of 100 microns, is located at the center of the posterior pole where it forms a slight depression centered on the fovea and the foveola. It has a 1,200-micron diameter. Within the macular area fluorescein angiography, we observe the avascular area that has a diameter of 450–500 microns and is sharply highlighted by the dye in the capillary phase. This dark avascular area is delimited by a continuous ring of fine anastomoses of the perifoveal vascular network, consisting of a single layer of capillaries.
The fovea itself, which is anatomically an area with a larger concentration of cones, is contained within a concentric circle having a diameter of 350 microns, hence it lies inside the fluorescein angiographic avascular area, while the foveola that corresponds to the macular center, measures about 100 microns. In the macula, there is a strong density of xanthophyllic pigment and at this level the cells of the pigment epithelium are higher and contain a bigger density of pigment granules. Apart from the absence of rods, the other specific feature of the macula is the decreased thickness of the retina and the thickening of the inner nuclear layers at the macula margins.
Around the macula area, the retina is 350 microns thick. Let us recall the nine layers of the retina: from the inner layer toward the outer layer, we find the internal limiting membrane, the nerve fibers layer, ganglion cells layer, inner plexiform layer, inner nuclear layer (bipolar cell bodies), outer plexiform layer, outer nuclear layer (cones and rods cellular bodies), outer limiting membrane, cones and rods layer. Then there is the external retinal layer consisting of a single layer of pigmented epithelial cells in close contact with each other through their “tight junctions”. These pigment epithelium cells are linked to each other and to Bruch's membrane or to the lamina vitrea by a cementing substance. The lamina vitrea is part of the choroid that is divided into choriocapillaris and choroid proper.
 
RETINAL ARTERIES AND VEINS
From the optic disk, take origin of the retinal arteries that form an arcade encircling the macula. Nerve fibers and central veins enter the optic disk. Arteries supply the inner layers of the neurosensory retina. A ciliary artery fills before the other retinal arteries. As the choroidal lobules it receives blood directly from the short posterior ciliary arteries (Figure 1).
The sensory retina thickness is supplied by two separate vascular systems. The inner side is supplied by retinal vessels; the most important branches are located in the nerve fiber level and form a loose network whereas the capillaries are observed in the inner half of the retina up to the inner nuclear layer and form a closer-knit network. The outer third of the retina instead is supplied by the choroid vascular system.
 
RETINAL PERIPHERY
Peripheral retina is generally subdivided into three zones:
  1. The mid-periphery, outside the vascular arcades
  2. The far-periphery, between equator and ora serrata, where the vortex veins are located
  3. The ora serrata or extreme periphery
In the periphery, the retina is less thick and has simpler structure. Neurons are bigger and scarcer.
zoom view
Figure 1: Retina periphery. Peripheral retina is subdivided into three zones. (1) The mid-periphery, outside the vascular arcades; (2) the far-periphery, between equator and ora serrata, where the vortex veins are located; and (3) the ora serrata or extreme periphery.
4
 
OPTIC DISK
The optic disk has a diameter of 1,500 microns whereas the retinal veins at the border of the disk have a maximum diameter of about 120 microns. At the mid-periphery, their diameter is about 60 microns. The retinal arteries have a slightly smaller diameter (respectively 80 and 50 microns). The capillaries in immediate contact with the retinal vessels are very scarce and virtually absent (periarterial avascular area). At the arteriovenous crossings, arteries and veins are united by a common adventitia. The size of retinal capillaries ranges between 5 and 10 microns.
 
THE CHOROID-VORTEX VEINS
The choroid is part of the vascular tunica of the eye and consists of dense vascular tissue where the larger vessels are positioned externally, close to the sclera (Haller layer), the smaller vessels are in the inner part (Sattler layer), and the choriocapillaris is in contact with the retina.
The choroid is supplied by the posterior ciliary arteries (about 15–20 branches). The vascular supply to the choroid is schematized in Figure 2 that indicates the districts supplied by each branch of the short and long posterior ciliary arteries. The districts are clearly separated from each other and form distinct wedges or triangles (Figure 2).
This figure helps to understand the fluorescein angiographic aspect of certain occlusive lesions of the choroid (triangular syndromes). The most important vessels are impermeable to fluorescein and are in contact with the sclera. They are visible on the fluorescein angiography in the presence of sclerosis of the choriocapillaris and of the retinal pigment epithelium (window lesions). The arteries subdivide rapidly forming lobules, small, irregular, distinct independent, and not interlinked units. Each unit or lobule is functionally independent from the others. The lobule measures about 250 × 300 microns. All the lobules together form the choriocapillaris whose capillaries are larger in size than other capillaries (20 microns) and they have fenestrated walls that allow the fluorescein to rapidly diffuse. The choriocapillaris provides nutrition and oxygen to the outer third of the retina (pigment epithelium, cones and rods).
zoom view
Figure 2: Choroid vascular supply. Choroid is supplied by the posterior ciliary arteries (from Hayreh, modified) – vascular districts form distinct wedges or triangle.
The veins of the choroid, originating from each lobule, flow into the 4 or 6 vortex veins located in the four quadrants of the bulb at the equator.