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6.3 Other Causes ofNew Vessels ontheRetina
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Fig. 6.20 Familial Exudative Vitreoretinopathy (FEVR).
A 12-year-old female patient with FEVR Stage 2A in the
right eye (a) and Stage 4B in the left eye (b). Ultra-wide
eld fundus uorescein angiography documents the presence of extra-retinal neovascularisation with a large area
with no genetic background and a consistent history of prematurity, low birth weight, and history
of oxygen therapy at birth. Family history may be
available in less than 20% of the FEVR patients.
Examination of the parents often reveals features consistent with FEVR [136]. Most of the
family members have stage 1 or 2 lesions which
are asymptomatic stages of the disease, while 3/4
of the patients show stage 3–5 lesions [137, 138].
Ultra-wide scanning laser ophthalmoscopy of the
asymptomatic family members can be highly
of temporal capillary non-perfusion (c and d). (Images
courtesy of Dr. Simar Rajan Singh, Advanced Eye Centre,
Post Graduate Institute of Medical Education and
Research, Chandigarh)
sensitive to detect early stages [139], and a temporal midperipheral vitreoretinal interface abnormality, prominent in the green channel may be
detected in the majority of the early stages of
FEVR [140]. Peripheral avascular retina on FFA
is one of the most consistent features of FEVR
and is seen in both the patients and the family
members.
Besides the non-perfused retina, wide-angle
FFA may show circumferential vessels, venous
anastomosis, telangiectasia, and leakage from the
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6 New Vessels ontheOptic Disc andElsewhere intheRetina
optic disc and peripheral vessels [137, 138]. On
spectral domain OCT, a key feature of FEVR is
the presence of the thickening of the posterior
hyaloid, causing a varying amount of vitreoretinal and vitreopapillary traction. The other important element of OCT is the persistence of the fetal
microstructures in the foveal centre, such as the
ganglion cell layer, inner plexiform layer, inner
nuclear layer, and outer plexiform layer. Other
changes include cystoid macular oedema, and
intraretinal or subretinal lipid exudation [141].
The role of laser photocoagulation of the peripheral avascular retina is controversial as the course
of the disease is unpredictable. However, patients
in stages 4 and 5 need vitreoretinal surgery, which
is challenging, although multiple surgeries may
ultimately reattach the retina in nearly 80% of the
patients [142] (Fig.6.21).
Genetic testing and counselling of the patients
and their family members of childbearing age are
essential to look for genetic mutations. The progression of this disease is unpredictable, and they
need a lifelong follow-up.
6.3.3 Sickle Cell Retinopathy
Sickle cell disease (SCD) is a generic term that
includes, among other genotypes, the commonest
form, sickle cell anaemia, which is an autosomal
recessive disorder caused by a point mutation in
the β-globin chain of haemoglobin [143]. The
disease is characterized by episodes of severe
pain and affects practically all body organs due to
an occlusive microvascular disease.
Microvascular occlusion is best appreciated clinically in the retina. Proliferative sickle cell retinopathy is one of the most common causes of
blindness in young people in Sub-Saharan Africa,
especially in Jamaica. SCD is caused by abnormal polymerization of haemoglobin S during
deoxygenation, leading to sickling. The disease
is named after the peculiar crescent and sickle
shape of the RBCs rst observed by Herrick
[144], who also noted anaemia and many
nucleated RBCs in the peripheral blood of a
young black student originally from Grenada
(West Indies) who suffered multiorgan involve-
ef
Fig. 6.21 The same patient as in Fig.6.20 was managed
with laser photocoagulation of the avascular retina in the
right eye (e) and scleral buckling with external drainage of
subretinal uid with cryotherapy in the left eye (f).
(Images courtesy of Dr. Simar Rajan Singh, Advanced
Eye Centre, Post Graduate Institute of Medical Education
and Research, Chandigarh)
6.3 Other Causes ofNew Vessels ontheRetina
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127
ment following the occurrence of episodes of
skin and ear infection [144].
6.3.3.1 Genetics ofSickle Cell Disease
The disease severity depends upon the genetic
variants. The most common allele is homozygous
βs responsible for the severest form of sickle cell
anaemia (HbSS) in nearly 70% of African SCD
patients. The next common variant is heterozygous βs βC alleles that cause less severe systemic
disease (HbSC). The third common is coinheritance with the β-thalassemia allele resulting in
HbS/ β-thalassemia disease [145].
6.3.3.2 Pathophysiology ofSickle Cell
Disease
The rigidity of RBCs is caused by the amount of
HbS available for polymerizing its β globin
chains that ll the RBC. Patients co-inheriting
genes that allow fetal Hb to persist have less
severe disease as the quantum of HbS available
for polymerization is reduced. Recent years have
seen the application of CRISPR/Cas9 gene editing tools to induce fetal haemoglobin expression
in these patients [146]. Initial clinical results have
been encouraging [147, 148]. The two primary
components of the disease are recurrent episodes
of occlusion of post-capillary veins and haemolytic anaemia precipitated by infections. Each
episode of infection leads to exacerbation of ischaemic events in different organs of the body.
Unlike 120days as the life span of normal RBCs,
the life span of RBCs is reduced to just 14days in
SCD, causing hemolysis and release of free haemoglobin [149] The free haemoglobin is toxic as
it leads to the generation of oxy free radicals,
which quench endothelial nitric oxide, a critical
molecule that controls vasodilatation. Oxidative
stress is also brought about by reperfusion injury
as the blood ow stops and restarts intermittently
in the capillaries. Apart from occlusion of the
post-capillary venules by the sickled RBCs, activation of endothelial cell adhesion molecules
VCAM by the oxidative stress and the inammatory cytokines contribute to the vascular occlusion by adhesion of RBCs and leucocytes.
6.3.3.3 Clinical Manifestations ofSickle
Cell Disease
While the HbSS disease has the severest forms of
systemic complications, the ocular complications
are severest in the HbSC variant [150].
While some of the earliest cases reported vitreous hemorrhage in patients with SCD, denitive ocular changes and their correlation with the
type of SCD were given by Welch and Goldberg
in [151]. Nearly 3/4 of the patients with HbSS
and HbSC show retinal changes. In general, no
retinal signs are seen in patients with Sickle cell
trait (HbAS).
Nearly half of the patients with HbSS disease
show tortuosity of the retinal veins, a stellate, and
speculated pigmented scar with feeder arterioles
and arteriolar occlusions, the so-called ‘black
sunburst sign’. These are accompanied by peripheral non-perfusion and arteriolar infarction.
Proliferative retinopathy is seen only occasionally. On the other hand, in the HbSC disease,
nearly 3/4th of the patients have abnormal arteriovenous proliferation into the vitreous cavity,
which has been described as ‘sea-fan vascularization’ along with arteriolar and venous segment
occlusions. All the sea-fan new vessels have
peripheral retinal capillary non-perfusion [151].
6.3.3.4 Classication ofProliferative
Sickle Cell Retinopathy
Goldberg [152] rst described ve stages of proliferative SCR in HbSC disease based primarily
on clinical and FFA studies of the retinal vascular
changes at the equatorial or post-equatorial retina. These were Stage I, peripheral arteriolar
occlusion; Stage II, arteriovenous anastomosis;
Stage III, sea fan neovascular and brous proliferation; Stage IV, vitreous hemorrhage, and Stage
V, retinal detachment. Each stage was further
sub-classied based on circumferential involvement [152]. Based on a prospective study of the
Jamaican Sickle cohort, a classication based on
the qualitative assessment of the vascular border
into type I and type II was proposed, limited,
however, by the inability of the then FFA technology to study the extreme peripheral vascular bed
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6 New Vessels ontheOptic Disc andElsewhere intheRetina
in all eyes. However, this study showed that the
retinopathy’s severity was more in the SC variant
than in the SS variant [153].
6.3.3.5 Fundus Imaging Studies
inSickle Cell Disease
In some of the earliest studies using FFA, a
dynamic remodelling of the retinal vessels, equatorial or post-equatorial venous segment dilations, dilated capillaries, capillary occlusion,
hairpin loops, A-V shunts, and capillary budding
had been noted. In a 3-year prospective study, a
continuous remodelling of the macular capillaries was noted [154]. This dramatic phenomenon
of intermittent ow cessation and reperfusion
was recently demonstrated on OCT angiography
of the retina by taking sequential OCTA images
every minute for 10min and then repeating these
after an hour at the same site. As the images were
stacked, the capillaries that showed intermittent
ow decit or started reperfusion could be identied and quantied [155]. Availability of the
ultra-wide-eld (UWF) FFA revealed more
extensive peripheral vascular changes than were
possible with the 7-standard eld fundus imaging
in SCR [156]. More recently, using UWF FFA,
100% of the pediatric age group patients with
SCD were shown to have at least stage I of the
Goldberg classication [157]. Even for screening
SCD patients, UWF color imaging is more sensitive than the dilated fundus examination [158].
UWF imaging can monitor SCR patients for progression, tele- screening, and machine learning
development [150]. Using a deep learning classier, UWF imaging can accurately distinguish
between various proliferative retinopathies in up
to 90% of the cases [159].
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