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25 Fundus Photography
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a
b
c
Fig. 25.14 Pathological myopia. (a) Myopic CNVM
(yellow circle) is seen as a grayish lesion at the macula.
(b) Lacquer cracks (yellow arrow) are seen as hyper-
25.7 Conclusion
Fundus photography is useful for documenting
and monitoring progress during treatment and
telemedicine, patient education, and academic
purposes. However, it requires good judgment to
reective lines on IR imaging. (c) The ultra-wide eld
image shows lattice degeneration (asterisk)
use the correct imaging mode and FOV; this var-
ies according to the clinical condition of the
patient and the requirements for the enhanced
visualization of the pathology. It is an essential
and indispensable tool for an ophthalmologist if
used wisely.
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A. Kulkarni et al.
Funding Hyderabad Eye Research Foundation,
Hyderabad, India.
Disclosure TYYL: Consultant: Allergan, Bayer,
Boehringer Ingelheim, Iveric Bio, Novartis, Oculis,
Roche; Speaker: Alcon, Bayer, Chendu Kanghong
Biotech, Novartis, Roche. Other authors: Nil
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Dye-Based Angiography
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AshwiniKulkarni , TimothyY.Y.Lai ,
SimonK.H.Szeto , andNirojKumarSahoo
26
26.1 Introduction
The evaluation of retinal disorders and retinal
imaging has evolved from using crude instruments in fundoscopy to dye-based imaging
techniques. At present, high-resolution imaging
of retinal and choroidal vessels is possible with
modern, high-quality fundus cameras, digital
imaging, and photographic lters. Fluorescein
angiography (FA) is an efcient tool for evaluating retinal circulation, and indocyanine green
angiography (ICGA) offers a more precise resolution of the choroidal circulation. In this
chapter, we will highlight the basics of retinal
imaging, equipment, techniques of FA and
ICGA, image analysis, and their clinical
implications.
A. Kulkarni
Kode Venkatadri Chowdary Campus, LV Prasad Eye
Institute, Vijayawada, India
T. Y. Y. Lai · S. K. H. Szeto
Department of Ophthalmology and Visual Science,
The Chinese University of Hong Kong, Faculty of
Medicine, Pok Fu Lam, Hong Kong
e-mail: tyylai@cuhk.edu.hk
N. K. Sahoo (*)
Anant Bajaj Retina Institute, Kode Venkatadri
Chowdary Campus, L V Prasad Eye Institute,
Vijayawada, India
26.2 Fundus Fluorescein
Angiography
26.2.1 History
In 1954, Edward Maumenee used fluorescein
dye intravenously to study ocular vasculature
in choroidal hemangiomas with a Goldmann
slit lamp, contact lens, and a cobalt blue filter.
Later, Chao and Flocks gave the earliest
description of fluorescein angiography (FA) in
1958 by studying its circulation time in cats
[1]. Novotny and Alvis (1961) gave a detailed
description of the fundus camera used for FA
with the filter details and technique of FA that
remains relatively unchanged to date [2].
Indocyanine green angiography (ICGA) was
initially developed for cardiologists for the
measurement of cardiac output accurately
(Kodak Research Laboratories) [3], and in
1972, Flower and Hochheimer were the first to
use intravenous ICGA to visualize the human
choroid [4]. Yannuzzi and colleagues demonstrated a 1024-line resolution system that was
synthesized with the proper flash synchronization and image- storing capability for high-resolution, long- duration ICGA [5]. Advances in
developing high-quality photography equipment, photographic filters, newer printing
techniques, and digital imaging can now generate high-resolution retina and choroid
angiography.
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2024
T. Das, P. Satgunam (eds.), Ophthalmic Diagnostics, https://doi.org/10.1007/978-981-97-0138-4_26
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26.2.2 Technology
26.2.2.1 Basic Principle
The emission of light from any source other than
a high-temperature source is called luminescence. When a luminescent material absorbs light
energy, a few electrons are elevated into a higher
energy state. These electrons decay spontaneously into lower energy states by emitting an
equivalent amount of energy as light. When this
emitted energy is within the visible light spectrum (400–700 nm), it is called luminescence.
Fluorescence is a type of luminescence that is
maintained only by continuous excitation.
Phosphorescence is a type of luminescence that
emits light even after the excitation is stopped. In
uorescence, excitation occurs at one wavelength, and emission occurs through a longer
wavelength [6, 7].
26.2.2.2 Sodium Fluorescein
Sodium uorescein is an orange-red crystalline
hydrocarbon with a molecular weight of 376.27
Daltons. It is a water-soluble dye; the liver and
kidney eliminate it within 24–36 h [7]. During
FA, intravenously injected Sodium uorescein
(Na Fl) remains 80% bound to proteins, and the
remaining 20% circulates freely in the bloodstream. The unbound dye has an excitation peak
in the blue range of the visible spectrum with
peak absorption at 465–490nm. In a ash-based
fundus camera, a blue excitation lter allows
only the blue light to enter the retina and absorbs
all other light. Fluorescein in the bloodstream,
excited by blue light, emits green-yellow light at
520–530nm. A barrier lter placed in front of the
lm allows only green-yellow light to be captured electronically as a digital image and lters
out the blue excitation light [6].
has a shorter learning curve. A digital camera
captures a single image of the retina using ashlight illumination and captures true-color images
of the retina.
26.2.2.4 Stereo Photography
Stereo photography allows in-depth stereoscopic
interpretation of images of both eyes simultaneously taken from slightly different angles [8]. A
slight change in angle causes the illuminating
beam of the fundus camera to pass through the
opposite slopes of the cornea. This results in
cornea- induced parallax that gives a hyperstereoscopic effect (see Chap. 25 for further
details) [9].
26.2.2.5 Camera andAncillary
Equipment
Filters: The exciter lter transmits blue light at
465–490 nm (absorption peak of uorescein),
and the barrier lter transmits light at 525–
530nm (emitted peak of uorescein) (Fig.26.1).
Newer digital fundus cameras use high-sensitivity monochrome sensors with excitation (580nm)
and barrier lters (695nm) of longer wavelengths
to overcome lens autouorescence [7, 10].
The eld of view in wide eld imaging (WFI)
is beyond 60–100°. The eld of view in ultrawide eld imaging (UWFI) is up to 200° and can
image over 80% of the retinal surface (see Chap.
25 for further details).
26.2.2.6 Confocal Scanning Laser
Ophthalmoscope
The confocal scanning laser ophthalmoscope
(cSLO) can be used for several retinal imaging
modalities, such as FA, ICGA, and fundus autouorescence (FAF). Refer to Chap. 25 for further
details.
26.2.2.3 Imaging
Digital imaging has replaced traditional lmbased imaging and is commonly used in FA. It
offers multiple advantages, such as higher image
resolution, ease of analysis, better storage, and
instant access to images. It also aids in image
reproducibility, image export for telemedicine,
and better patient education. Digital imaging also
26.2.3 Techniques
26.2.3.1 Fundus Fluorescein
Angiography
Written informed consent is taken after the procedure is explained to the patient. The patient’s
pupils are dilated to facilitate imaging of the
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Fig. 26.1 The absorption (465–490nm) and emission (at 525–530nm) spectrum of uorescein dye
Table 26.1 Essential supplies for uorescein angiography
Supply Description Purpose
Catheter 23g scalp vein needle or
22g intravenous catheter
Syringe 5mL disposable To administer dye
Dye (Na Fl) 10mL of 5% (500mg) or
5mL of 10% (500mg) or
3mL of 25% (750mg)
Needle 20g, 1 ½ inch needle To withdraw the dye
Tourniquet Stretchy latex-free/latex-based/ with
velcro closure
Alcohol swab 60–70% isopropyl alcohol or ethanol,
single-use swab, or cotton wool ball
Adhesive tape Nonsterile micropore paper tape/
transpore polyethylene tape
Gloves Latex/nitrile/vinyl To maintain asepsis
Emergency medicine Antihistamines, atropine, adrenaline,
corticosteroids, etc.
For intravenous dye administration
To visualize retinochoroidal vasculature
To help localize peripheral veins to achieve
successful venipuncture
To disinfect the skin surface before IV
cannulation
For securing the IV cannula
For quick administration of drugs in case of
adverse reactions
329
peripheral retina. The primary eye to be examined should be correctly identied and positioned
for proper alignment, focus, and comfort. The FA
tray (Table26.1) should be kept ready. Color fundus photographs and monochromatic red-free lter images are obtained before the dye is
administered. Before injecting the dye, the angiographer should pre-focus the area of interest. A
bolus injection of the dye is administered into the
upper limb vein via a small gauge scalp vein needle or intravenous catheter (Fig.26.2). The angiographer should start the timer as soon as the dye
is injected and begin capturing images immediately thereafter to capture the choroidal ush and
early arteriovenous phase (every 1–2 s in the
early phase). The arm-to-retina circulation time
is usually 10–12s in normal individuals and up to
20s in older individuals. During the early phase,
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Fig. 26.2 (Left) Patient positioning during the FFA procedure. (Right) Buttery needle with uorescein dye
A. Kulkarni et al.
images of only one eye can be captured.
Photographs of other parts of the retina in the primary and fellow eyes are obtained as soon as the
early phase is complete. The examiner should use
his/her judgment to follow a particular order in
capturing various areas of interest as required in
the specic case. At the end of the procedure, the
patient should be re-informed that his/her urine
and skin may have orange discoloration due to
the dye. Na Fl may be administered orally at
25mg/kg body weight in children with difcult
IV access. Fundus images are captured 40–60min
after dye ingestion, but the quality of images is
generally suboptimal [11].
26.2.3.2 Side Eects
andComplications
Mild side effects of Na Fl dye usage are nausea,
vomiting, and minimal extravasation of the dye;
generally, these subside with time without any
specic treatment. Moderate side effects include
pruritis, urticaria, syncope, thrombophlebitis,
pyrexia, and local tissue necrosis; these require
medical intervention, and patients usually recover
well. Severe adverse reactions include anaphylaxis, shock, laryngeal edema, bronchospasm,
myocardial infarction, and convulsions; these
require intensive treatment. Very few cases of
death have been reported, with an estimated risk
of death of less than 1in 220,000 [12].
26.2.3.3 Contraindications
An absolute contraindication for FA is a known
allergy or a history of severe adverse reactions
during previous uorescein dye injection. The
dye can be used cautiously in advanced renal
failure patients on regular dialysis, and the dose
of uorescein injection can be reduced to half.
Intradermal testing of diluted Na Fl can be done
in selected cases [7]. The presence of heart disease, arrhythmias, or cardiac pacemakers are not
contraindications. No fetal complications from
uorescein injection during pregnancy have been
reported yet. However, it is generally best to
avoid angiography in pregnant women, especially in the rst trimester. Fluorescein dye has
been detected for up to 72h in breastmilk after IV
administration. To limit neonatal exposure, the
US Food and Drug Administration suggests that
nursing mothers should “pump-and-dump” the
breastmilk for at least 96 h after uorescein dye
injection [13].
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26.2.4 Clinical Application
andInterpretation
the other. The foveal avascular zone (FAZ) is 400–
500μm in diameter and represents the area of the
macula devoid of any retinal capillaries.
26.2.4.1 Basic Anatomical
Considerations
The ophthalmic artery divides into two main
branches of posterior ciliary arteries: the lateral
and medial, which supply the lateral and medial
portions of the disc and choroid. A vertical zone of
slightly delayed lling may be seen during angiography, which traverses the disc and the papillomacular area. This zone demarcates the border
between the two main posterior ciliary arteries. It
26.2.4.2 Normal Fluorescein
Angiography
FA is a serial analysis of the vascular structure of
the choroid and retina over specic time intervals. Fluorescein dye enters the ocular circulation
through the short posterior ciliary arteries, which
supply the choroid, and the central retinal artery
that supplies the retina.
The six phases of FA are listed in Table26.2.
is called the “watershed zone,” and patchy choroidal lling is often seen during FA within this zone.
The ciliary arteries supply most of the disc; thus,
uorescein is rst seen at the optic nerve head and
the choroid before it is seen in the retinal artery
system. The choriocapillaris has a lobular arrangement and demonstrates patchy lling in a transverse manner, with one lobule spilling over into
Table 26.2 Fluorescein angiography phases and their appearances
FA phases Time (normal eye) Appearance
Prearterial (choroidal
ush)
Arterial 10s 1–2s after the choroidal ush, the central retinal artery lls, and
Arteriovenous Complete lling of the arteries and capillaries is followed by an
Venous phase Fluorescein lling in the veins increases; the two parallel laminae
Transit phase The transit phase is the rst complete passage of blood containing
Recirculation phase or
late phase
10min The uorescein is gradually emptied from the choroidal and
Choriocapillaris and the bigger choroidal vessels start to ll with
dye. Fluorescein is seen in the choroidal circulation around 1s
earlier than in the retinal circulation
the dye ows into the retinal arterioles (Fig.26.3a). The avascular
zone of the fovea is generally hypouorescent due to the presence
of taller, more pigmented RPE cells, xanthophyll pigment, and the
absence of retinal capillaries in the center of the fovea
initial laminar ow in the vein (Fig.26.3b). The plasma that
contains unbound uorescein ows along the vessel wall. The
blood ow is faster in the center of the lumen. This differential
ow rate of the different blood components creates the laminar
venous ow pattern
along the wall steadily get thicker and eventually meet to form a
broad uorescein dye column in the retinal veins (Fig.26.3c). The
dye in the posterior ciliary vascular system uoresces both from
the edge of the disc and the tissue between the center and
circumference of the disc. Numerous capillaries of the central
retinal artery on the surface of the disc ll up, making the disc
hyperuorescent on the angiogram
uorescein through the choroid and retina. The macula has the
quickest transit time, and the peripheral retina has a longer transit
time
retinal vasculature, and the vessels turn gray 3–5min after the
injection (Fig.26.3d)
26.2.4.3 Abnormal Fluorescence
Angiography
Abnormal uorescence [7, 14] is primarily of
two types: hypouorescence and hyperuorescence. Hypouorescence is a reduction/absence
of normal uorescence, and hyperuorescence
means increased uorescence.
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a
c
b
d
Fig. 26.3 Normal phases of FA. (a) Arterial phase with
background choroidal ush. (b) Arteriovenous phase. (c)
Venous phase. (d) Late phase: the retinal arteries are
Fig. 26.4 Causes of hypouorescence
A. Hypouorescence
Hypouorescence refers to an abnormally dark area on the angiogram. It can be
caused by blocked uorescence or a vascu-
beginning to empty. Pooling can be seen temporal to the
macula due to a pigment epithelial detachment
lar lling defect (Figs. 26.4 and 26.5;
Table26.3).
B. Hyperuorescence (Figs. 26.6 and 26.7;
Table26.3)
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Hyperuorescence is the abnormal
increase in uorescence and can be classied as [1] pre-injection uorescence, [2]
transmitted uorescence, [3] abnormal vessels, [4] leakage, and [5] staining
(Fig.26.6).
ab
ab
Fig. 26.5 Left upper panel: Blocked retinal uorescence
due to retinal hemorrhage (the yellow arrow in the color
fundus image (left) and FA (right)) (Image courtesy:
Navya Cherukuri, MD). Left lower panel: Blocked choroidal uorescence (yellow circle) due to congenital
hypertrophy of retinal pigment epithelium (CHRPE in the
Table 26.3
FA appearance Category Mechanism Common examples
Hypouorescence Vascular lling
Interpretation and clinical application of uorescein angiography
defects
Blocked
uorescence
Vascular obstruction,
absence of vessels
Reduction/absence of
normal retinal or choroidal
uorescence due to tissue,
blood, or uid barrier
located anterior to it
color fundus image (left) and FA (right)) (Image courtesy:
Rajeev K Reddy Pappuru, MD). Right panel:
Hypouorescent capillary non-perfusion area (white
arrow) with hyperuorescence due to leakage from retinal
neovascularization (yellow arrow). (Image courtesy:
Hitesh Agrawal, MD)
Retina: Central or branch artery occlusion,
capillary non-perfusion in DR (diabetic
retinopathy), RVO (retinal vein occlusion).
Choroid: Malignant hypertension, toxemia,
lupus choroidopathy
Retina: Vitreous hemorrhage, inammatory
debris, vitreous membranes, retinal
hemorrhage. Choroid: Any uid, exudate,
hemorrhage, or scar present deep to the retina
and in front of the choroidal vasculature
result in blocked choroidal uorescence
(continued)
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