CENTRAL RETINAL VEIN OCCLUSION

ASSOCIATED WITH CILIORETINAL

ARTERY OCCLUSION
SOHAN SINGH HAYREH, MD, PHD, DSC, FRCS, FRCOPHTH,*
LYNN FRATERRIGO, MD,* JOST JONAS, MD†

Purpose: To describe the clinical characteristics and pathogenesis of central retinal vein
occlusion (CRVO) associated with cilioretinal artery occlusion (CLRAO).
Methods: The study included 38 patients (38 eyes) who had CRVO associated with
CLRAO and were seen in our clinic from 1974 to 1999. At their first visit to our clinic, all
patients provided a detailed ophthalmic and medical history and underwent comprehen-
sive ophthalmic evaluation, color fundus photography, and fluorescein fundus angiogra-
phy. At each follow-up visit, the same ophthalmic evaluations were performed, except for
fluorescein fundus angiography.
Results: Of 38 eyes, 30 had nonischemic CRVO, 5 had ischemic CRVO, and 3 had
nonischemic hemi-CRVO. Patients with nonischemic CRVO were significantly younger (mean
age ⫾ SD: 45.3 ⫾ 16.0 years) than those with ischemic CRVO (72.3 ⫾ 9.2 years; P ⫽ 0.001)
and those with nonischemic hemi-CRVO (64.7 ⫾ 7.5 years; P ⫽ 0.018). At least one third of the
patients gave a definite history of episode(s) of transient visual blurring before the onset of
constant blurred vision. Initially, the ophthalmoscopic and fluorescein angiographic findings
were similar to those seen in CRVO and hemi-CRVO, except that all these eyes had retinal
infarct in the distribution of the cilioretinal artery; its size and site varied widely. Fluorescein
angiography typically showed only transient hemodynamic block and not the typical CLRAO.
During follow-up, visual acuity improved markedly in nonischemic CRVO (P ⬍ 0.001) and
nonischemic hemi-CRVO but deteriorated in ischemic CRVO. Retinopathy resolved sponta-
neously in 22 eyes with nonischemic CRVO (mean duration ⫾ SD: 42.0 ⫾ 101.0 months), in 2
eyes with ischemic CRVO (15.4 ⫾ 4.5 months), and in 1 eye with nonischemic hemi-CRVO.
Retinociliary collaterals developed in 30% of eyes with nonischemic CRVO, in 40% of eyes
with ischemic CRVO, and in 66% of eyes with nonischemic hemi-CRVO.
Conclusion: CRVO associated with CLRAO constitutes a distinct clinical entity. The
pathogenesis of CLRAO in CRVO is due to transient hemodynamic blockage of the
cilioretinal artery caused by a sudden sharp rise in intraluminal pressure in the retinal
capillary bed (due to CRVO) above the level of that in the cilioretinal artery.
RETINA 28:581–594, 2008

C entral retinal vein occlusion (CRVO) is a common

visually impairing condition. Some eyes with
CRVO, at its onset, may have associated cilioretinal
artery occlusion (CLRAO). Oosterhuis1 in 1968 and
Hayreh2 in 1971 first reported this condition (one case
From the *Department of Ophthalmology and Visual Sciences, Col-
lege of Medicine, University of Iowa, Iowa City, USA; and the †Depart-
ment of Ophthalmology and Eye Hospital, Medical Faculty Mannheim of
the Ruprecht-Karls-University Heidelberg, Mannheim, Germany.
Supported by grant EY-1576 from the National Institutes of
Health and in part by unrestricted grants from Research to Prevent
Blindness, Inc. (New York, NY).
each). Since then, there have been many anecdotal case
reports, and some series included as many as 4 to 11
eyes, with data collected retrospectively.3–9 The two
largest reported series were of 11 eyes by McLeod and
Ring4, from 4 British hospitals, and of 10 eyes by Schatz
et al6, from 10 different institutions. This reflects the
The authors have no proprietary interest in this study.
Reprint requests: Sohan Singh Hayreh, MD, Department of
Ophthalmology and Visual Sciences, University of Iowa Hospitals
& Clinics, 200 Hawkins Drive, Iowa City, IA 52242-1091; e-mail:
sohan-hayreh@uiowa.edu

581
582 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
rarity of this condition. One of us (S.S.H.) had seen two
cases of nonischemic CRVO with CLRAO (in 19682 and
in 1970). On the basis of that experience, we started to
study this clinical entity in 1974 as a part of our prospec-
tive study on CRVO at the Ocular Vascular Clinic of the
University of Iowa Hospitals & Clinics (Iowa City). On
the basis of our series of 38 eyes, we describe the clinical
characteristics and pathogenesis of CRVO associated
with CLRAO.
Materials and Methods
This study was a part of our prospective study on
ocular vascular occlusive disorders, funded by the
National Institutes of Health (RO1). From 1974, we
investigated systematically, in detail, eyes with CRVO
associated with simultaneous onset of CLRAO, to
ascertain its various clinical characteristics and patho-
genesis. Up to 1999, 38 eyes with CLRAO and CRVO
or hemi-CRVO10 were seen in our clinic.
Inclusion Criteria
In all eyes, presence of CLRAO with CRVO or
hemi-CRVO must have been documented by ophthal-
moscopy and/or fluorescein angiography at our clinic
or by the referring ophthalmologist (in one case).
Diagnostic Criteria for CRVO and Hemi-CRVO
Pathogenetically, CRVO and hemi-CRVO are iden-
tical in nature.10
CRVO
Our experimental and clinical studies have shown
that CRVO consists of two distinct clinical entities:
nonischemic CRVO and ischemic CRVO.11,12 CRVO
was categorized as nonischemic or ischemic on the
basis of the combined data acquired from visual acuity
measurement, analysis of visual fields (measured with
a Goldmann perimeter), relative afferent pupillary de-
fect testing, electroretinography, ophthalmoscopy, and
fluorescein fundus angiography, as discussed in detail
elsewhere.11,12
Hemi-CRVO
This variant of CRVO10 also consists of two distinct
entities: nonischemic hemi-CRVO and ischemic
hemi-CRVO. Criteria to define these two types are
reported elsewhere.10
Examinations Performed
At the initial visit, all patients were seen by one of
us (S.S.H.) at the Ocular Vascular Clinic; a detailed
● 2008 ● VOLUME 28 ● NUMBER 4
ocular and medical history was obtained, and a de-
tailed bilateral ocular examination was performed. We
obtained a full medical history of all previous or
current systemic diseases. The ocular examination in-
cluded testing of the visual function using the Snellen
visual acuity chart, Amsler grid, and visual field plot-
ting with a Goldmann perimeter (I-2e, I-4e, and V-4e
isopters), anterior segment examination, intraocular
pressure recording with a Goldmann applanation
tonometer, relative afferent pupillary defect testing,
fundus evaluation by indirect and direct ophthalmos-
copy and if required by contact lens, and fluorescein
fundus angiography (only for the involved eye). In
addition to these evaluations, most patients had sys-
temic and hematologic evaluations either by an inter-
nist at the University of Iowa Hospitals & Clinics or
by their local internists.
During follow-up, ocular evaluations (performed
by S.S.H.) were the same as those described above,
except for fluorescein fundus angiography, which
was repeated only when considered essential. When
clinical findings were suggestive of ischemic CRVO,
electroretinography was usually performed during the
initial visit to differentiate nonischemic from ischemic
type; if a change in status of CRVO from nonischemic
to ischemic was suspected, it was repeated. The pa-
tients were observed according to a protocol: at ap-
proximately three monthly intervals for three visits,
then six monthly intervals for four visits, and yearly
after that.
To determine whether the visual fields improved,
deteriorated, or stayed stable, all the visual fields
plotted during the entire follow-up period were laid
out in chronologic order. Evaluation of the entire
visual field and evaluation of central and peripheral
fields were carried out separately. In general, deterio-
ration was defined as development of a new scotoma,
a deepening or expanding scotoma, a generalized con-
striction not accounted for by any other ocular param-
eter, or overall deterioration. Improvement was the
reverse of the above. Subtle changes were confirmed
at more than one examination. The entire visual field
was graded into four levels: from 0 (normal) to 4
(severe loss) in steps of 0.5 (and occasionally 0.25
when the differences were subtle), with recording of
the dates when each change was noted during the
entire follow-up. The grade was judged by qualita-
tively assessing clinical computation of the amount of
visual field loss, factoring in the functional disability
produced by that defect. We have found this method
to provide reliable evaluation in several other studies
in the past.13–15
 CRVO ASSOCIATED WITH CLRAO ● HAYREH ET AL 583

Data Analysis Demographic Characteristics

Statistical analysis was performed using a commer-
Table 1 summarizes the demographic character-
cially available statistical software package (SPSS for
istics of the 38 eyes. In the nonischemic CRVO
Windows, version 14.0; SPSS, Chicago, IL). The data
group, one patient had developed nonischemic
are given as mean ⫾ SD. ␹2 Tests were used to compare
CRVO in the fellow eye in the past, one woman
proportions. Logistic regression was used to investi-
gave a history of using oral contraceptives, and one
gate the associations of the binary dependent variable
patient had systemic vasculitis. The follow-up pe-
with the continuous or categorical independent vari-
riod according to the three types of CRVO is given
ables, such as age and sex. Confidence intervals were
in Table 1.
presented. All P values were two sided and were
There was a difference in the age at onset in the
considered statistically significant when P ⬍ 0.05.
three groups. In the nonischemic CRVO group, age
(mean ⫾ SD, 45.8 ⫾ 16.0 years; range, 19 – 80 years)
Results
was significantly younger than in the ischemic CRVO
In this study of CLRAO associated with CRVO or group (72.3 ⫾ 9.2 years; P ⫽ 0.001; 95% confidence
hemi-CRVO, there were 38 eyes: 30 with nonisch- interval [CI], ⫺37.9 to ⫺15.0) and the nonischemic
emic CRVO, 5 with ischemic CRVO, and 3 with hemi-CRVO group (64.7 ⫾ 7.5 years; P ⫽ 0.02; 95%
nonischemic hemi-CRVO. CI, ⫺33.1 to ⫺4.7).

Table 1. Demographic and Clinical Features of Eyes With CRVO

Nonischemic Ischemic Nonischemic
Parameter CRVO (n ⫽ 30) CRVO (n ⫽ 5) Hemi-CRVO (n ⫽ 3)
Age (y)
Range 19–80 60–85 59–73
Median 41.4 70.7 61.3
Mean ⫾ SD 45.3 ⫾ 16.0 72.3 ⫾ 9.2 64.7 ⫾ 7.5
Males 13 2 3
Right eyes 16 2 3
CLRAO diagnosis initially based on
Clinical evaluation 26 4 3
Fluorescein angiography 1 0 0
Both 3 1 0
Glaucoma 3 1 0
Ocular hypertension 5* 0 0
Systemic history
Hypertension 5 3 0
Diabetes 0 0 0
Ischemic heart disease 2 2 0
Stroke 0 1 1
Smoking
Persons smoking 12 1 2
Mean no. of pack years of smoking ⫾ SD 35 ⫾ 30 10 9⫾1
Amaurosis fugax episode(s) before visual loss 11 2 1
Time of onset of blurred vision
Upon awakening from sleep 7 1 2
Morning 3 1 1
Forenoon 7 1 0
Afternoon 7 2 0
Evening 2 0 0
Unknown 4 0 0
Progressive visual loss 6 1 0
Systemic corticosteroid therapy 7 0 0
Follow-up (mo)
Median 37.9 35.0 10.9
Mean ⫾ SD 63.9 ⫾ 74.0 33.6 ⫾ 20.7 63.5 ⫾ 100.2
Unless stated otherwise, data are no. of eyes.
*Pigment dispersion syndrome in 2 eyes and pseudoexfoliation in 1 eye.
CRVO, central retinal vein occlusion; CLRAO, cilioretinal artery occlusion.
584 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES ● 2008 ● VOLUME 28 ● NUMBER 4

Table 2. Initial and Final Visual Acuities

Nonischemic Ischemic Nonischemic
CRVO (n ⫽ 30) CRVO (n ⫽ 5) Hemi-CRVO (n ⫽ 3)

Visual Acuity Initial Final Initial Final Initial Final

20/15 to 20/25 10 23 0 0 1 1
20/30 to 20/40 4 4 0 0 1 1
20/50 to 20/60 7 1 0 0 0 1
20/70 to 20/100 3 0 0 1 0 0
20/200 0 0 1 0 0 0
20/400 to hand motions 6 2 4 3 1 0
Light perception to no light perception 0 0 0 1 0 0
Data are no. of eyes.
CRVO, central retinal vein occlusion.

Visual Symptoms hemi-CRVO. Table 2 summarizes the initial and final

Table 1 summarizes the visual symptom findings.
Initial visual symptoms in all three groups were
caused by sudden development of CLRAO; although
in some eyes, there may have been additional visual
deterioration from macular edema caused by CRVO
or hemi-CRVO.
In at least one third of cases, there was a definite
history of episode(s) of transient visual blurring before
the onset of constant blurred vision. The duration of
amaurosis fugax in the nonischemic CRVO group
varied from ⬇15 minutes to 30 minutes (mean ⫾ SD,
23.7 ⫾ 7.5 minutes). During the episode, the patients
saw purple or lavender haze and occasionally orange
spots. Some patients had multiple episodes. There was
no definite time pattern when these episodes of am-
aurosis fugax developed. In the ischemic CRVO
group, one patient had a purple lacy curtain over
vision during the episode; another had intermittent
episodes for 6 weeks before permanent visual loss.
Sudden onset of visual blurring was discovered
more often in the morning or forenoon, usually when
the patient first tried to use fine vision, than at other
times of the day, and in two cases of nonischemic
CRVO, it occurred after a syncopal episode. During
follow-up, patients often complained that vision was
worse in the morning and gradually improved during
the day. An occasional patient noticed further deteri-
oration of vision on awaking in the morning. In the
nonischemic CRVO group, slowly progressive visual
loss after the initial visual loss was reported by six
patients (after 1 day in one, 2 days in two, 4 days in
one, 3 weeks in one, and unknown in one).
Visual Acuity
Initial deterioration of visual acuity in all the three
groups may be due to either CLRAO involving the
foveal region or macular edema caused by CRVO or
visual acuity findings in the three groups. Visual acuity at
baseline of the study was worse in the ischemic CRVO
group (mean ⫾ SD, 0.25 ⫾ 0.20) than in the nonisch-
emic CRVO group (0.51 ⫾ 0.39) and the nonischemic
hemi-CRVO group (0.49 ⫾ 0.43; P ⫽ 0.39).
Using the criterion of a vision change of at least ⱖ2
Snellen lines as a significant change, eyes in the
nonischemic CRVO group had a marked (mean in-
crease ⫾ SD, 0.40 ⫾ 0.46) and significant (P ⬍ 0.001;
95% CI, 0.22– 0.57) visual acuity improvement during
follow-up, as is evident from the findings in Table 2.
In the nonischemic CRVO group, the visual acuity
improvement usually tended to occur fairly quickly
without any treatment; for example, of eyes seen
within 1 week after the initial visit, 1 had vision
change from hand motion to 20/20 within 4 days, 1
had vision change from counting fingers to 20/40
within 5 days, and 3 had vision change from counting
fingers or 20/400 to 20/20, 20/25, and 20/40 within 6
days. The nonischemic hemi-CRVO group had a sim-
ilar pattern (mean increase ⫾ SD, 0.18 ⫾ 0.27). By
contrast, in the ischemic CRVO group, visual acuity
deteriorated during follow-up (mean loss ⫾ SD, 0.17 ⫾
0.24). In the nonischemic hemi-CRVO group and in
the ischemic CRVO group, the number of patients was
too small to calculate a statistical significance of the
change in visual acuity during follow-up.
In addition, in the nonischemic hemi-CRVO group,
two of three eyes had visual acuity improvement: one,
from 20/30 to 20/20; and one, from counting fingers to
20/60. None of the eyes in the ischemic CRVO group
had any improvement.
Seven of 30 patients in the nonischemic CRVO
group were treated with oral systemic corticosteroid
therapy: either it was started by the referring ophthal-
mologist, or the patient volunteered to receive it in our
clinic. In this small sample of treated eyes, the gain in
 CRVO ASSOCIATED WITH CLRAO ● HAYREH ET AL 585

visual acuity did not vary significantly from that in Table 3. Visual Field Defects at the Initial Visit
untreated patients (P ⫽ 0.22; 95% CI, ⫺0.16 – 0.63). Type of Visual
Visual acuity deterioration during follow-up was Field Defect, Nonischemic Ischemic Nonischemic
invariably due to development or worsening of mac- No. of Eyes CRVO CRVO Hemi-CRVO
ular edema secondary to CRVO or hemi-CRVO, and Total 30 5 3
not from CLRAO (which inflicts damage only at its Central 4 2 1
onset). In the ischemic CRVO group, there was further scotoma
visual deterioration in three of five eyes (due in two Centrocecal 13 3 0
cases to development of neovascular glaucoma). scotoma
Paracentral 4 0 1
scotoma
Visual Fields Inferior 1 0 0
arcuate
We evaluated visual fields by Amsler chart testing and defect
plotting of visual fields with a Goldmann perimeter. Inferior 4 0 1
nasal
Initial Defects by Amsler Chart Testing defect
Superior 1 0 0
In the nonischemic CRVO group, there was a cen- altitudinal
tral defect in 15 eyes, a paracentral defect in 12, and defect
no detectable defect in 3. Temporal 1 0 0
sector
defect
Visual Field Defects None 2 0 0
Table 3 lists the various types of visual field defect CRVO, central retinal vein occlusion.
seen at the initial visit and their incidence in the three
groups. Like visual acuity, visual field improvement
was common in the nonischemic CRVO group, except patients (e.g., 14 vs 51 mmHg in 1 eye, 16 vs 30
in eyes where an area of the retina had had irreversible mmHg in 1, 12 vs 22 mmHg in 1, and 10 vs 16 mmHg
ischemic damage. In the nonischemic CRVO group, in 1).
overall clinical assessment of the visual fields showed
that central visual fields improved in 21 eyes, re- Vitreous
mained stable in 4, and worsened in 2, with no data for
the remaining 3 eyes; in the nonischemic hemi-CRVO At the initial visit, there were some cells in the
group, the central field improved in two of three eyes vitreous (a common finding in our studies on various
and remained stable in one eye. Our visual field eval- types of retinal vein occlusion): 12 eyes with nonisch-
uation in both nonischemic CRVO and nonischemic emic CRVO, 2 with ischemic CRVO, and 1 with
hemi-CRVO groups showed normal peripheral fields nonischemic hemi-CRVO. One of the eyes with non-
in all eyes initially as well as finally, except in six eyes ischemic CRVO had asteroid hyalosis.
where segmental visual field loss (inferior nasal in
four, superior altitudinal in one, and temporal sector in Optic Disk Changes
one; Table 3) was the result of occlusion of a large
At the initial visit, the optic disk was edematous in
cilioretinal artery, supplying a large segment of the
all eyes except 3 (2 eyes with nonischemic CRVO and
retina, that caused ischemic damage in that region and
1 with ischemic CRVO) and had hemorrhages on it
resulted in peripheral visual field loss.
(22 with nonischemic CRVO, 3 with ischemic CRVO,
and 2 with nonischemic hemi-CRVO); the severity of
Anterior Segment
disk edema varied from mild to marked. The optic
At the initial visit, findings of anterior segment disk developed pallor (in the region of the retinal
evaluation were within normal limits except for one infarct) in 20 eyes with nonischemic CRVO, 4 with
eye with ischemic CRVO that had iris neovascular- ischemic CRVO, and 2 with nonischemic hemi-
ization. In the nonischemic CRVO group, the intraoc- CRVO. Retinociliary collaterals were seen at clinic
ular pressure usually was ⱖ2 mmHg lower in the visits 1.5 months to 10 months (mean ⫾ SD, 5.2 ⫾ 3.0
involved eye (mean ⫾ SD, 15.7 ⫾ 4.2 mmHg) than in month; median, 4.2 months) after onset in 9 eyes with
the fellow normal eye (17.9 ⫾ 6.8 mmHg), with a nonischemic CRVO, after 4 months and 5.5 months in
marked difference in intraocular pressure between the 2 with ischemic CRVO, and 3.5 months and 5 months
involved eye and the fellow normal eye in a few in 2 with nonischemic hemi-CRVO.
586 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES ● 2008 ● VOLUME 28 ● NUMBER 4

Retinal Infarction Caused by CLRAO
Table 4 lists the size of the involved cilioretinal arter-
ies and the area and extent of the retina involved by the
retinal infarct caused by their occlusion in the three
groups. Usually, cilioretinal arteries supplied a narrow
retinal strip of variable length temporal to the optic disk
(Fig. 1A); however, in some eyes, it supplied a much
larger area of the retina (Fig. 1B). For example, in the
nonischemic CRVO group, the cilioretinal artery sup-
plied almost the entire lower half of the retina in one eye
(Fig. 1B), the superotemporal quadrant in two, and a
sector nasal to the optic disk in one.
The cilioretinal artery may or may not supply the
foveal region, and when it does, it may supply the
entire fovea or only one part of it. In the present study,
when the cilioretinal artery supply did not reach the
fovea, the retinal infarct caused by CLRAO was at a
variable distance from the edge of the fovea: nonisch-
emic CRVO group, 0.25 disk diameter (DD), ⬍0.5
DD, 0.5 DD, 1 DD, 1 DD, 1.5 DD, 2 DD, and ⬎2 DD
in 8 eyes; ischemic CRVO group, 1 DD and 1.5 DD in
2 eyes; and nonischemic hemi-CRVO group, 0.75 DD
in 1 eye. In six eyes in the nonischemic CRVO group,
the infarct touched the fovea above in one eye, nasally
in one eye, and at the lower border in two eyes and
touched the foveola in two eyes (Fig. 1); in one
nonischemic hemi-CRVO eye, the infarct touched the
superior part of the fovea. When the foveal retina was
involved by the infarct, the part involved depended
upon the location of the cilioretinal artery, which may
run horizontally between the disk and the fovea or
above or below the horizontal line. When there was a
tiny or small cilioretinal artery, then it involved only
either the peripapillary retina or a small area adjacent
but away from the fovea. The retinal opacity caused
by infarction was usually more marked in the foveal
region, and at resolution, the opacity in that region
tended to be the last to resolve. We found that some of
the tiny CLRAOs had been misdiagnosed ophthalmo-
scopically as “cotton-wool spots.” In a few eyes, there
was a white crescentlike opacity at the tip of the
cilioretinal artery supply, due to axoplasmic flow ob-
struction. Later on, the cilioretinal artery developed
sheathing in some eyes.
Retinal Changes Due to CRVO or Hemi-CRVO
In all three groups of this study, apart from the
retinal infarct caused by the CLRAO, the various

Table 4. Retinal Infarction Caused by Cilioretinal Artery Occlusion

Nonischemic Ischemic Nonischemic
Retinal Infarct, No. of Eyes CRVO (n ⫽ 30*) CRVO (n ⫽ 5) Hemi-CRVO (n ⫽ 3)
Size of the occluded artery
Large 6 0 1
Medium 15† 2 1
Small 7 3 1
Tiny 2 0 0
Foveal involvement by infract
Entire fovea 2 1 0
Upper half 2 0 0
Superior nasal part 1 0 1
No involvement 24 4 2
Infarct touches
Fovea 4 2 1
Foveola 2 0 0
Vertical height of infarct in disk diameters
0.75 3 1 0
1 12 2 1
1.25 3 0 1
1.5 3 1 0
2 2 0 0
2.5 1 0 0
4.0 0 1 0
Involves large area of the retina 6‡ 0 1§
*One of 30 eyes was not seen during the acute phase.
†One eye had 2 medium-sized cilioretinal arteries.
‡Almost entire lower half of retina in 1, entire superotemporal quadrant in 2, a sector nasal to the optic disk in 1, and difficult
to define in 2.
§Involved entire superotemporal quadrant of the retina.
CRVO, central retinal vein occlusion.
 CRVO ASSOCIATED WITH CLRAO
Fig. 1. Two examples showing the distribution and size of the retinal
infarct with cilioretinal artery occlusion in eyes with nonischemic
central retinal vein occlusion. A, Infarct only in a narrow strip below
the foveola. B, Infarct involving most of the lower half of the retina.
retinal changes were typically those seen in CRVO
and hemi-CRVO. These consisted of initially
engorged and tortuous retinal veins, retinal hemor-
rhages, macular edema, and, in some eyes, cotton-
wool spots. All these retinal findings progressively
underwent changes during follow-up. The following
is a summary of the important retinal changes seen
in these eyes.
Retinal Venous Changes.—In the three groups, all
eyes had variable degrees of venous engorgement
during the acute phase. One eye in a 24-year-old with
nonischemic CRVO had perivenous exudation due to
retinal phlebitis at onset. At the final visit, perivenous
sheathing was seen in six eyes with nonischemic
● HAYREH ET AL 587
CRVO, one with ischemic CRVO, and one with non-
ischemic hemi-CRVO.
Retinal Hemorrhages.—At the initial visit, the pres-
ence and severity of retinal hemorrhages were evalu-
ated separately in the peripapillary, foveal, central,
and peripheral areas of the retina. In nonischemic
CRVO, ischemic CRVO, and nonischemic hemi-
CRVO, retinal hemorrhages were seen in the peripap-
illary region in 17, 4, and 2 eyes, respectively, in the
foveal area in 6, 2, and 0 eyes, respectively, in the
macular region in 29, 5, and 3 eyes, respectively, and
in the periphery in 29, 5, and 3 eyes, respectively. The
hemorrhages gradually resolved with time; the time
varied widely from eye to eye.
Macular Retinal Changes.— Table 5 lists the various
macular changes seen at the initial visit and during
follow-up. When the CLRAO involved the central
macular region, a cherry-red spot was seen. In a few
eyes seen early, swelling of the peripheral nasal foveal
retina, associated with retinal infarction, caused lifting
up of the adjacent normal foveolar retina and visual
acuity deterioration.
Cotton-Wool Spots.—During the early stage, cotton-
wool spots were present in 12 of 30 eyes with non-
ischemic CRVO, 1 of 5 with ischemic CRVO, and 0
of 3 with nonischemic hemi-CRVO. These lesions
were mostly located in the temporal arcade regions
and, in some eyes, the peripapillary area.
Fluorescein Fundus Angiography Findings
Angiography was performed on all eyes in this
series; however, for some eyes, its quality was not
good enough to supply all the information we needed.
There was sometimes poor quality for a variety of
reasons, or the initial stages of angiography required
for evaluation of cilioretinal artery circulation were
unsatisfactory or missing because of poor cooperation
from the patient. Angiographic findings were divided
into two categories.
Related to CLRAO.—Relevant data related to
cilioretinal artery circulation by angiography in this
study are summarized in Table 6. For many of these
eyes, the angiography was performed by one of us
(S.S.H.), providing information about the dynamics of
blood flow in the eye, not obtained from routine
angiography. This showed that during the early stages
of the transit of the dye, the cilioretinal artery in these
eyes filled for a variable distance from the optic disk
during systole but the filling retracted to the optic disk
during diastole, resulting in an oscillating blood col-
umn in the cilioretinal artery, extending back and forth
from the optic disk into the retina.
588 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES ● 2008 ● VOLUME 28 ● NUMBER 4

Table 5. Macular Changes

Nonischemic CRVO Ischemic CRVO Nonischemic Hemi-CRVO
Macular Change (n ⫽ 30) (n ⫽ 5) (n ⫽ 3)
At initial visit*
Edema and severity
Marked 0 3 0
Moderate 2 0 0
Mild 5 0 2
None 22 2 1
Foveolar cyst 5 3 1
Later on during follow-up
Epiretinal membrane 2 1 1
RPE degeneration 3 1 0
Cystoid degeneration 1 0 0
*One of 30 eyes was not seen during the acute phase.
CRVO, central retinal vein occlusion; RPE, retinal pigment epithelium.

Related to CRVO or Hemi-CRVO.—These eyes also Resolution of Retinopathy

had the well-known angiographic abnormalities seen
in eyes with CRVO or hemi-CRVO. The interval
between the start of filling of the retinal arteries and
that of the retinal veins (i.e., retinal arteriovenous
transit time) was very much prolonged: 7.7 ⫾ 3.6
seconds in nonischemic CRVO and 7.7 ⫾ 5.7 seconds
in ischemic CRVO. During the late phase of angiog-
raphy, optic disk staining was most common, less
common than that was perivenous staining, and mac-
ular staining was least common.
In this study, during follow-up at our clinic, the reti-
nopathy resolved in 22 of 30 eyes with nonischemic
CRVO, in 2 of 5 with ischemic CRVO, and in 1 of 3
with nonischemic hemi-CRVO. In eyes where the reti-
nopathy resolved, it took a mean ⫾ SD of 42.0 ⫾ 101.0
months (median, 8.1 months; range, 0.7– 472.3 months)
in nonischemic CRVO and 15.4 ⫾ 4.5 months (median,
15.4 months; range, 12.2–18.6 months) in ischemic
CRVO. The higher mean of the resolution time for the

Table 6. Fluorescein Fundus Angiography Findings

Nonischemic Ischemic Nonischemic
Finding CRVO (n ⫽ 30*) CRVO (n ⫽ 5) Hemi-CRVO (n ⫽ 3)
Delayed filling of CLRA
Yes 20 3 2
No 6 2 1
No filling 2 0 0
No data 2 0 0
Interval between central retinal artery and CLRA filling
No filling 2 0 0
Retrograde flow 2 0 0
Delayed filling† 17 2 1
No delay 5 2 0
No data 4 1 2
Total time it took for CLRA to fill completely
No filling 2 0 0
Delayed filling 20‡ 2 2
Normal 2 2 0
No data 6 1 1
Capillary foveal arcade
Intact 25 0 3
Broken 3 3 0
No data 2 2 0
Data are no. of eyes.
*One of 30 eyes was not seen during the acute phase.
†Three eyes, 1 second (s); 4 eyes, 2 s; 1 eye, 3 s; 1 eye, 5 s; 8 eyes, delay time not known.
‡Three eyes, 2 s; 1 eye, 3 s; 3 eyes, 4 s; 2 eyes, 6 s; 1 eye, 7 s; 2 eyes, 8 s; 1 eye, 9 s; 1 eye, 10 s; 1 eye, 17 s; 1 eye, 19 s; 4 eyes,
marked delay.
CRVO, central retinal vein occlusion; CLRA, cilioretinal artery.
 CRVO ASSOCIATED WITH CLRAO
nonischemic type than for the ischemic type may be a
statistical artifact due to the low number of patients in the
subgroup.
Discussion
Clinical Characteristics of CRVO Associated With
CLRAO
This comprehensive description of this clinical en-
tity is based on our study of 35 eyes with CRVO (30
eyes with nonischemic CRVO and 5 with ischemic
CRVO) and 3 eyes with hemi-CRVO, all associated
with development of CLRAO. Patients in the nonisch-
emic CRVO group were significantly younger than
those with ischemic CRVO and hemi-CRVO (P ⬍
0.001 and P ⫽ 0.018, respectively) (Table 1). In our
study, the age range in the nonischemic CRVO group
was 19 years to 80 years (median, 41.4 years), in
contrast to the patients in the studies by Schatz et al6
(10 cases) and Keyser et al8 (4 cases) who were all
younger than 50 years of age.
At least one third of the patients in the present study
gave a definite history of episode(s) of transient visual
blurring before the onset of constant blurred vision
(Table 1). Only an occasional patient, of ⬇1,000 pa-
tients with ordinary CRVO and hemi-CRVO seen in
our clinic since 1973, has given such a history. This
indicates that a history of episode(s) of transient visual
blurring before the onset of constant blurred vision
constitutes an important diagnostic feature of this clin-
ical entity.
Deterioration of visual acuity in all three groups
might have been due to either occlusion of the
cilioretinal artery per se, when it involved the foveal
region, or macular edema caused by CRVO or hemi-
CRVO; initially, it was usually due to CLRAO pro-
ducing a visual field defect. Eyes in the nonischemic
CRVO group without foveal involvement by CLRAO
(80%; Table 4) had a marked visual acuity improve-
ment during follow-up; however, when the retinal
infarct involved the foveal zone, it resulted in perma-
nent central scotoma (Table 3). Overall visual acuity
improvement in the nonischemic CRVO group was
similar to that seen in eyes without any CLRAO,16 in
spite of the associated CLRAO. It is important to point
out that when the infarct caused by CLRAO or a
branch retinal artery touches the fovea (Fig. 1), ini-
tially visual acuity deterioration may simply be due to
swelling of the foveal retina caused by the infarct,
which lifts up the adjacent normal foveolar retina; in
these eyes, visual acuity improves spontaneously
within a few weeks with resolution of the infarct,17
and that frequent spontaneous occurrence may be mis-
● HAYREH ET AL 589
takenly attributed to various treatments.18 In contrast
to nonischemic CRVO, in ischemic CRVO, although
4 (80%) of 5 eyes had no foveal involvement by the
CLRAO (Table 4), there was no similar visual acuity
improvement (Table 2); this was because foveal reti-
nal ganglion cells usually had irreversible ischemic
damage at the onset of ischemic CRVO, irrespective
of foveal involvement by CLRAO. That basic differ-
ence between ischemic and nonischemic CRVO was
responsible for the difference in visual acuity change
during follow-up in the two types of CRVO. In the
ischemic CRVO group, there was further visual dete-
rioration in three of five eyes (in two cases due to
development of neovascular glaucoma).
The type of visual field defect caused by CLRAO
varied widely. Centrocecal scotoma is the most com-
mon type and almost diagnostic of CLRAO. Apart
from central scotoma, which in some eyes might
have been caused by macular edema due to CRVO,
the type and severity of visual field defects depend
upon the following: the size, location, and distribu-
tion of the occluded cilioretinal artery; the severity
and duration of retinal ischemia (see below); and the
time between the onset of CLRAO and the evaluation.
In eyes with mild retinal ischemia initially, a part of
the ischemic area may have already recovered visual
function by the time a patient is seen, leaving only a
central or paracentral scotoma instead of a centrocecal
scotoma. Like visual acuity, visual field improvement
was common in the nonischemic CRVO group, except
in eyes where an area of retina had had irreversible
ischemic damage. Central visual fields improved in
70% of eyes with nonischemic CRVO. Peripheral
visual fields in both nonischemic CRVO and nonisch-
emic hemi-CRVO eyes were normal in all initially as
well as finally, except in six where segmental visual
field loss (Table 3) was the result of occlusion of a
large cilioretinal artery, supplying a large segment of
the retina.
CRVO and hemi-CRVO usually cause a fall (ⱖ2
mmHg) of intraocular pressure in the involved eye, by
some unknown mechanism. 19 There is a high preva-
lence of glaucoma or ocular hypertension among
CRVO and hemi-CRVO eyes. 19 In this study as well
as in our large CRVO study, we have seen that when
an eye with ocular hypertension develops CRVO,
often the intraocular pressure drops to normal levels.
Therefore, the presence of normal intraocular pressure
in the involved eye does not necessarily rule out
glaucoma or ocular hypertension in the fellow unin-
volved eye.19 In view of that, treatment of ocular
hypertension or glaucoma in the fellow eye is crucial
to reduce the risk of that eye developing CRVO or
hemi-CRVO.
590 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
Initially, the ophthalmoscopic fundus findings were
similar to those seen in CRVO and hemi-CRVO,
except that these eyes had retinal infarct in the distri-
bution of the occluded cilioretinal artery (which may
or may not involve the foveal region) (Table 4). The
ophthalmoscopic fundus findings due to CRVO, as
usual, consisted of engorged retinal vein, optic disk
edema, retinal hemorrhages, and macular edema (Ta-
ble 5). During follow-up, retinociliary collaterals de-
veloped in 30% (9 of 30) of eyes with nonischemic
CRVO within 1.5 months to 10 months (median, 4.2
months) after onset, in 40% (2 of 5) of eyes with
ischemic CRVO within 4 months to 5.5 months of
onset, and in 66% (2 of 3) of eyes with nonischemic
hemi-CRVO within 3.5 months to 5 months of onset.
Fluorescein fundus angiography provides useful in-
formation for these eyes with CLRAO. Normally, the
cilioretinal artery starts to fill just before the central
retinal artery at the optic disk, although in some eyes
the cilioretinal and central retinal arteries start to fill at
the same time. However, in eyes with CRVO associ-
ated with CLRAO, the filling pattern of the cilioretinal
artery depends upon the time between the onset of
visual symptoms and fluorescein angiography. When
the eyes were seen shortly after the onset, they had a
classical oscillating blood column in the cilioretinal
artery (i.e., the artery filled for a variable distance
from the optic disk during systole but the filling re-
tracted to the optic disk during diastole). However,
when the eyes were seen a few days after the onset of
symptoms, the cilioretinal artery started to fill: the
shorter the time interval (i.e., greater the retinal ve-
nous stasis), the longer it took the artery to fill. Table
6 provides information about the delay in filling of the
cilioretinal artery when the patients were first seen in
the clinic, which in most cases was not at onset; this
delay in filling may be misinterpreted to mean that in
our study the CLRAOs were most often not total. That
extent of delay depends upon the speed with which
the venous collaterals developed in the optic nerve
and the time between the onset of visual symptoms
and the first clinic visit (and angiography), which
also varied widely among the patients.
Our studies on CRVO and hemi-CRVO have shown
that the retinopathy resolves spontaneously in due
course in all eyes. In this study, during follow-up, the
retinopathy resolved in 73% (22 of 30) of eyes with
nonischemic CRVO in 35.1 ⫾ 101.7 months, in 40%
(2 of 5) of eyes with ischemic CRVO in 121.2 ⫾
210.5 months, and in 33% (1 of 3) of eyes with
nonischemic hemi-CRVO. In the rest, the follow-up
was not long enough.
In our studies on CRVO, we have found that not
every eye with cilioretinal artery develops occlusion
● 2008 ● VOLUME 28 ● NUMBER 4
and retinal infarct after CRVO. In our Ocular Vascular
Clinic, we have investigated CRVO and hemi-CRVO
in a large cohort of patients since 1973. In a prelimi-
nary analysis of a cohort of the first 465 alphabetically
consecutive patients with CRVO (406 nonischemic
CRVO cases and 59 ischemic CRVO cases), we eval-
uated the eyes that had cilioretinal artery, but there
was no evidence of its occlusion, on the basis of
ophthalmoscopic, angiographic, and visual field eval-
uations. Of the nonischemic CRVO eyes, 8% (32 of
406) had cilioretinal arteries without any occlusion;
their sizes varied widely: tiny in 13 eyes (in 2 eyes, 2
arteries), small in 15 (in 1 eye, 2 arteries), medium
sized in 2, and large in 2 (in 1 eye, it supplied the
entire upper half of the retina). However, only 1 of 59
eyes with ischemic CRVO without any occlusion had
a cilioretinal artery of small size.
Pathogenesis of Simultaneous Development of
CLRAO in Eyes With CRVO or Hemi-CRVO
Several hypotheses have been put forward to ex-
plain the simultaneous development of CLRAO and
CRVO. McLeod and Ring4 postulated that in these
patients, “partial obstruction of their posterior ciliary
arteries may be the explanation for at least some of our
cases.” They went on: “This series may represent a
spectrum of ocular vascular lesions intermediate be-
tween acute central retinal vein occlusion and acute
ischemic optic neuropathy.” Glacet-Bernard et al5
stated that the pathogenesis of this condition remains
unclear and the possibility of primary occlusion of the
cilioretinal artery must be considered in these eyes. It has
also been proposed that optic disk edema caused by
CRVO can cause CLRAO. Some researchers have even
attributed CLRAO with CRVO to embolism. Schatz et
al6 discussed the various possible mechanisms.
To comprehend the pathogenesis of this clinical
entity, one must understand the factors that influence
the ocular blood flow. Blood flow in general depends
upon the intraluminal perfusion pressure (perfusion
pressure ⫽ arterial pressure ⫺ venous pressure). There-
fore, factors that either reduce the arterial pressure or
increase the venous pressure, or a combination of both,
result in reduced perfusion pressure and, consequently,
decreased blood flow or even no circulation.
There is a difference in the arterial supply and
venous drainage systems of the retina between eyes
with an additional cilioretinal artery and eyes with the
central retinal artery as the only source of blood sup-
ply. The venous drainage from the entire retina is by
the central retinal vein, irrespective of the numbers
and sources of the arteries that supply the retina. In
eyes with a cilioretinal artery, the arterial supply to
 CRVO ASSOCIATED WITH CLRAO
the retina is obviously from two independent sources:
the central retinal artery is the major source, and the
cilioretinal artery usually supplies only a small part of
the retina, but its distribution can vary widely.20 Oc-
casionally, the cilioretinal artery may supply one
quadrant or half of the retina; in our Ocular Vascular
Clinic, we have seen two patients who had an entire
retina supplied by the cilioretinal arteries with no
central retinal artery. The central retinal artery and
cilioretinal artery belong to two types of arterial sys-
tems with different physiologic properties. The central
retinal artery arises directly from the ophthalmic ar-
tery and has an efficient blood flow autoregulation, so
that when there is a fall in perfusion pressure in the
retinal arterial bed caused by a rise in the retinal
venous pressure, the autoregulatory mechanism in the
retinal arterial bed causes a rise in its pressure to try to
maintain retinal circulation. By contrast, because the
cilioretinal artery belongs to the choroidal vascular
system, the following two entirely different mecha-
nisms are working in the cilioretinal artery circulation
in eyes with CRVO: the choroidal vascular bed has no
autoregulation in it, and there is no vortex venous
obstruction. Therefore, with sudden onset of CRVO, a
decrease in perfusion pressure in the central retinal
artery kicks in the autoregulatory mechanism to main-
tain its blood flow; by contrast, no such compensatory
mechanism exists in the cilioretinal artery. Moreover,
studies have shown that the perfusion pressure in the
choroidal vascular bed normally is lower than that in
the central retinal artery.21–23 Thus, the theory that in
these eyes there is partial obstruction of their posterior
ciliary arteries and that this represents “a spectrum of
ocular vascular lesions intermediate between acute
central retinal vein occlusion and acute ischemic optic
neuropathy”4 is not valid; moreover, there is no evi-
dence of anterior ischemic optic neuropathy in these
eyes.
In the light of the above-mentioned facts, let us look
at the hemodynamic situation in eyes that have a
cilioretinal artery and develop CRVO. Sudden occlu-
sion of the central retinal vein results in a marked rise
of intraluminal pressure in the entire retinal capillary
bed; when that intraluminal pressure rises above that
in the cilioretinal artery, the result is a hemodynamic
block in the cilioretinal artery. For many of these eyes,
angiography performed during the early acute phase
provided information about the in vivo dynamics of
blood flow in the eye. During the early stages of the
transit of the dye, the cilioretinal artery in these eyes
usually filled up to the optic disk, because the optic
nerve head is supplied mainly by the posterior ciliary
arterial circulation.24,25 During systole, the cilioretinal
artery often filled for a variable length from the optic
● HAYREH ET AL 591
disk into the retina, but during diastole, the filling
retracted to the optic disk, resulting in an oscillating
blood column in the cilioretinal artery, moving back
and forth from the optic disk for a variable distance
into the retina. Thus, the CLRAO in these eye is
simply a hemodynamic block and not due to embolism
or thrombosis. The hemodynamic block is invariably
transient, lasting from a few hours to several days,
depending upon how rapidly the collateral circulation
is established by the central retinal vein through its
multiple tributaries in the optic nerve. Therefore, in
the optic nerve, the further anterior the site of occlu-
sion in the central retinal vein, the fewer are the
tributaries available, and the longer it takes to rees-
tablish the circulation, and vice versa. As soon as
those tributaries establish collateral circulation, there
is a fall of intraluminal pressure in the retinal capillary
bed to below that of the blood pressure in the cilioreti-
nal artery, resulting in restoration of retinal circulation
in the distribution of the cilioretinal artery. Hence, if a
patient with CRVO is seen for the first time many days
after the onset of CLRAO, a retinal infarct is present
ophthalmoscopically, but by angiography, there is no
evidence of CLRAO, which can result in confusion
and mistaken diagnosis of the cause of retinal infarct
(this may be why CLRAO is mistakenly attributed to
embolism). In hemi-CRVO, when one of the two
trunks of the central retinal vein is occluded, the
above-mentioned mechanism applies only to the seg-
ment of the retina drained by the occluded trunk.10
Nocturnal Arterial Hypotension
Patients with CRVO associated with CLRAO often
have the following complaint: visual loss is often first
discovered on waking up from sleep or in the morning
on first opportunity to use fine central vision (Table 1).
To comprehend the reason for this, one must con-
sider the important phenomenon of nocturnal arte-
rial hypotension.
Fall of blood pressure during sleep is a well-estab-
lished physiologic phenomenon. We have investigated
that by doing 24-hour ambulatory blood pressure
monitoring for ⬎700 patients, for whom blood pres-
sure was recorded every 10 minutes during the waking
hours and every 20 minutes during sleep. In our stud-
ies,26,27 we found that during sleep there is a fall of
systolic blood pressure by 34.8 ⫾ 1.2% and a fall of
diastolic blood pressure by 44.0 ⫾ 1.3% from daytime
blood pressures.27 This fall of blood pressure is ag-
gravated by overmedication with blood pressure–low-
ering medication, particularly when the medication is
given in the evening or at bedtime. There were two
other important relevant findings of our study. The
592 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES
most impressive finding of our 24-hour ambulatory
blood pressure monitoring study was that systemic
arterial blood pressure is the most volatile parameter
in the human body and is greatly influenced instanta-
neously by physical or emotional factors. Daytime
blood pressure usually has no relationship to nighttime
blood pressure (Fig. 2). Because blood pressure is
always evaluated based on daytime measurement,
there is almost invariably no information about blood
pressure during sleep. This is particularly true for a
patient who has just had visual loss and is emotionally
upset. In view of that, arterial hypertension discovered
in CRVO patients at the time of their diagnosis may be
of one of three types: genuine arterial hypertension;
temporary arterial hypertension due to emotional up-
set at sudden visual loss; or “white coat hypertension.”
Unfortunately, it is not unusual to find that a newly
seen CRVO patient who was found to have transient
arterial hypertension in his ophthalmologist’s office
may be treated aggressively by physicians without
realizing that the patient may not have genuine arterial
hypertension at all. This has the potential of precipi-
tating or aggravating the visual loss in CRVO eyes
with cilioretinal artery (see below) and also can con-
vert nonischemic CRVO to ischemic CRVO. Thus, an
understanding of nocturnal arterial hypotension has
important implications both for comprehension of the
mechanism of development of CLRAO with CRVO
and for management of these patients (see below).
Therefore, in eyes with CRVO and cilioretinal ar-
tery, the following sequence of events takes place: fall
● 2008 ● VOLUME 28 ● NUMBER 4
Fig. 2. Ambulatory blood
pressure (top) and heart rate
(bottom) monitoring record
(based on individual read-
ings) staring at 11 AM and go-
ing on until 10 AM the next
day.
of systemic blood pressure during the night, secondary
falls in the cilioretinal artery blood pressure (without
any appreciable change in the intraluminal pressure in
the retinal capillary bed caused by CRVO), hemody-
namic block in the cilioretinal artery during sleep, no
retinal circulation in its distribution for several sleep-
ing hours, and retinal infarct in the distribution of the
cilioretinal artery. Thus, a marked fall of blood pres-
sure during sleep may play an important role in the
development of CLRAO in these patients.
In at least one third of patients, there was a definite
history of episode(s) of transient visual blurring before
the onset of constant blurred vision (Table 1). This is
most probably also due to a transient fall in systemic
blood pressure during waking hours, for whatever
reason (e.g., orthostatic hypotension), resulting in a
transient hemodynamic block in the cilioretinal artery.
Naturally, the following question arises: Why did only
one third of the patients have transient vision blurring
before the onset of constant blurred vision and not all
patients? Whether a patient gets these episodes of
transient blurring before developing CLRAO depends
upon the difference between the intraluminal pressure
in the retinal capillary bed and that in the cilioretinal
artery (see above). There can be two scenarios. If the
difference between the two pressures is very small,
even a transient mild fall of systemic blood pressure is
enough to precipitate such an episode (e.g., with or-
thostatic hypotension). However, if that difference is
substantial, it would require, proportionately, a much
greater fall of systemic blood pressure (e.g., with
 CRVO ASSOCIATED WITH CLRAO
marked nocturnal arterial hypotension). In the latter
case, these episodes may be occurring during sleep,
but the patient is not aware of them.
As discussed above, there are eyes with a cilioreti-
nal artery that do not develop CLRAO with CRVO.
We have seen the following two types of cases.
Many patients, when first seen many days or weeks
after the onset of visual blurring, had no evidence of
infarction or any significant delay in filling of the
cilioretinal artery. In these eyes, obviously, the in-
traluminal pressure in the retinal capillary bed was
never high enough to interfere with cilioretinal artery
filling. This may be due to slow development of
CRVO, which allows time for collaterals to develop in
the optic nerve, so that the intraluminal pressure in the
retinal capillaries never gets high enough to cause
hemodynamic block in the cilioretinal artery. The
other possible explanation is that the cilioretinal artery
is a direct branch of the posterior ciliary artery20 and
is not a part of the choroidal vascular bed, so that it has
the same intraluminal pressure as the central retinal
artery (both arising from the ophthalmic artery).
We have also seen an occasional patient who pre-
sented soon after having developed transient visual
obscuration, with markedly engorged retinal veins and
none or a rare retinal hemorrhage. For these eyes,
angiography revealed markedly delayed filling of the
cilioretinal artery but no occlusion. This indicates that
in these eyes, although the intraluminal pressure in the
retinal capillary bed is high enough to cause delayed
filling of the cilioretinal artery, it is not high enough to
produce a complete hemodynamic block and infarc-
tion yet is high enough to produce transient visual
obscuration. This would indicate that delayed filling
of the cilioretinal artery is present much earlier than
development of complete hemodynamic block and
retinal infarction. Most likely, the retinal infarction
develops in these eyes when nocturnal arterial hypo-
tension during sleep causes intraluminal pressure in
the cilioretinal artery to fall below the critical level,
resulting in a hemodynamic block in the cilioretinal
artery that lasts many hours.
In two eyes in the present series, there was only
nonischemic CRVO at the initial visit, but at the next
follow-up visit, they were found to have developed
CLRAO some time during the intervening period,
indicating that CLRAO can occasionally develop later
on. In these cases, the cause was presumably the
development of an abnormal degree of nocturnal hy-
potension (from arterial hypotensive therapy or other
causes27), because the patients had visual loss on
waking in the morning.
From the management point of view, for patients
who present with any of the above-mentioned symp-
● HAYREH ET AL 593
toms or findings, it is essential to evaluate and regulate
their blood pressure–lowering medication, to prevent
further visual loss. Our 24-hour ambulatory blood
pressure monitoring studies have shown that patients
who are overmedicated with blood pressure–lowering
drugs or take those drugs in the evening or at bedtime
are highly susceptible to develop marked nocturnal
arterial hypotension27 and consequent visual loss.
To understand why some eyes with CRVO associ-
ated with CLRAO develop permanent visual loss in
the distribution of cilioretinal artery while others have
only temporary loss, it is essential to consider retinal
tolerance time to acute ischemia. Our studies have
shown that acute retinal ischemia lasting for up to
⬇100 minutes causes no irreversible retinal damage
and the retina recovers its function fully; however,
after that, the longer the acute ischemia, the greater the
irreversible ischemic damage.28,29 Eyes with 240 min-
utes of acute retinal ischemia have no recovery of
visual function.28,29 Therefore, in eyes with CRVO
associated with CLRAO, the severity of visual loss
and the recovery of retinal function depend upon the
duration and severity of retinal ischemia in the area of
retina supplied by the cilioretinal artery.
Strengths and Limitations of the Study
To our knowledge, the present study is the largest
study of CRVO associated with CLRAO. It includes
38 eyes, and all the patients were seen in the same
clinic, evaluated meticulously and followed by the
same investigator (S.S.H.). The imbalance in the num-
ber of eyes in the three groups of CRVO types in this
study may be considered by some a limitation; how-
ever, it roughly coincides with their overall incidence
in a much larger study30 on the incidence of various
types of CRVO.
Key words: central retinal vein occlusion, cilioreti-
nal artery occlusion, posterior ciliary artery, retinal
artery, retinal vein.
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