OVCR combinado OACR

8/6/2019 OVCR combinado OACR

1/14

CENTRAL RETINAL VEIN OCCLUSION

ASSOCIATED WITH CILIORETINALARTERY OCCLUSIONSOHAN 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 28:581594, 2008

Central retinal vein occlusion (CRVO) is a commonvisually impairing condition. Some eyes with

CRVO, at its onset, may have associated cilioretinalartery occlusion (CLRAO). Oosterhuis1 in 1968 and

Hayreh2 in 1971 first reported this condition (one case

each). Since then, there have been many anecdotal casereports, and some series included as many as 4 to 11

eyes, with data collected retrospectively.39 The twolargest reported series were of 11 eyes by McLeod and

Ring4, from 4 British hospitals, and of 10 eyes by Schatzet al6, from 10 different institutions. This reflects the

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 Mannheimofthe Ruprecht-Karls-University Heidelberg, Mannheim, Germany.

Supported by grant EY-1576 from the National Institutes ofHealth and in part by unrestricted grants from Research to PreventBlindness, Inc. (New York, NY).

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:[email protected]

581


2/14

rarity of this condition. One of us (S.S.H.) had seen two

cases of nonischemic CRVO with CLRAO (in 19682 andin 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 clinicalcharacteristics and pathogenesis of CRVO associatedwith CLRAO.

Materials and Methods

This study was a part of our prospective study on

ocular vascular occlusive disorders, funded by theNational Institutes of Health (RO1). From 1974, we

investigated systematically, in detail, eyes with CRVOassociated 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 thebasis of the combined data acquired from visual acuity

measurement, analysis of visual fields (measured witha Goldmann perimeter), relative afferent pupillary de-

fect testing, electroretinography, ophthalmoscopy, andfluorescein 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 ischemichemi-CRVO. Criteria to define these two types are

reported elsewhere.10

Examinations Performed

At the initial visit, all patients were seen by one ofus (S.S.H.) at the Ocular Vascular Clinic; a detailed

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-4eisopters), 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 fieldwas 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.1315

582 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2008 VOLUME 28 NUMBER 4


3/14

Data Analysis

Statistical analysis was performed using a commer-cially available statistical software package (SPSS for

Windows, version 14.0; SPSS, Chicago, IL). The dataare given as mean SD. 2 Tests were used to compare

proportions. Logistic regression was used to investi-gate the associations of the binary dependent variable

with the continuous or categorical independent vari-ables, such as age and sex. Confidence intervals were

presented. All P values were two sided and were

considered statistically significant when P 0.05.

Results

In this study of CLRAO associated with CRVO or

hemi-CRVO, there were 38 eyes: 30 with nonisch-emic CRVO, 5 with ischemic CRVO, and 3 with

nonischemic hemi-CRVO.

Demographic Characteristics

Table 1 summarizes the demographic character-

istics of the 38 eyes. In the nonischemic CRVOgroup, one patient had developed nonischemic

CRVO in the fellow eye in the past, one woman

gave a history of using oral contraceptives, and onepatient had systemic vasculitis. The follow-up pe-riod according to the three types of CRVO is given

in Table 1.There was a difference in the age at onset in the

three groups. In the nonischemic CRVO group, age(mean SD, 45.8 16.0 years; range, 1980 years)

was significantly younger than in the ischemic CRVOgroup (72.3 9.2 years; P 0.001; 95% confidence

interval [CI], 37.9 to 15.0) and the nonischemichemi-CRVO group (64.7 7.5 years; P 0.02; 95%

CI, 33.1 to 4.7).

Table 1. Demographic and Clinical Features of Eyes With CRVO

ParameterNonischemic

CRVO (n 30)Ischemic

CRVO (n 5)Nonischemic

Hemi-CRVO (n 3)

Age (y)Range 1980 6085 5973Median 41.4 70.7 61.3Mean SD 45.3 16.0 72.3 9.2 64.7 7.5

Males 13 2 3Right eyes 16 2 3CLRAO diagnosis initially based on

Clinical evaluation 26 4 3

Fluorescein angiography 1 0 0Both 3 1 0Glaucoma 3 1 0Ocular hypertension 5* 0 0Systemic history

Hypertension 5 3 0Diabetes 0 0 0Ischemic heart disease 2 2 0Stroke 0 1 1

SmokingPersons smoking 12 1 2Mean no. of pack years of smoking SD 35 30 10 9 1

Amaurosis fugax episode(s) before visual loss 11 2 1Time of onset of blurred vision

Upon awakening from sleep 7 1 2

Morning 3 1 1Forenoon 7 1 0 Afternoon 7 2 0Evening 2 0 0Unknown 4 0 0

Progressive visual loss 6 1 0Systemic corticosteroid therapy 7 0 0Follow-up (mo)

Median 37.9 35.0 10.9Mean 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.

583CRVO ASSOCIATED WITH CLRAO HAYREH ET AL


4/14

Visual Symptoms

Table 1 summarizes the visual symptom findings.Initial visual symptoms in all three groups were

caused by sudden development of CLRAO; althoughin some eyes, there may have been additional visual

deterioration from macular edema caused by CRVOor hemi-CRVO.

In at least one third of cases, there was a definitehistory of episode(s) of transient visual blurring before

the onset of constant blurred vision. The duration ofamaurosis 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 orangespots. 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 overvision 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 whenthe patient first tried to use fine vision, than at other

times of the day, and in two cases of nonischemicCRVO, it occurred after a syncopal episode. During

follow-up, patients often complained that vision wasworse in the morning and gradually improved during

the day. An occasional patient noticed further deteri-oration of vision on awaking in the morning. In thenonischemic CRVO group, slowly progressive visual

loss after the initial visual loss was reported by sixpatients (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 thefoveal region or macular edema caused by CRVO or

hemi-CRVO. Table 2 summarizes the initial and final

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 2

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, 0.220.57) 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 visionchange 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

Table 2. Initial and Final Visual Acuities

NonischemicCRVO (n 30)

IschemicCRVO (n 5)

NonischemicHemi-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 1 120/50 to 20/60 7 1 0 0 0 120/70 to 20/100 3 0 0 1 0 020/200 0 0 1 0 0 020/400 to hand motions 6 2 4 3 1 0Light perception to no light perception 0 0 0 1 0 0

Data are no. of eyes.CRVO, central retinal vein occlusion.



5/14

visual acuity did not vary significantly from that in

untreated patients (P 0.22; 95% CI, 0.160.63).Visual acuity deterioration during follow-up was

invariably due to development or worsening of mac-ular edema secondary to CRVO or hemi-CRVO, and

not from CLRAO (which inflicts damage only at its

onset). In the ischemic CRVO group, there was furthervisual deterioration in three of five eyes (due in twocases to development of neovascular glaucoma).

Visual Fields

We evaluated visual fields by Amsler chart testing and

plotting of visual fields with a Goldmann perimeter.

Initial Defects by Amsler Chart Testing

In the nonischemic CRVO group, there was a cen-

tral defect in 15 eyes, a paracentral defect in 12, and

no detectable defect in 3.

Visual Field Defects

Table 3 lists the various types of visual field defect

seen at the initial visit and their incidence in the threegroups. Like visual acuity, visual field improvement

was common in the nonischemic CRVO group, exceptin eyes where an area of the retina had had irreversible

ischemic damage. In the nonischemic CRVO group,overall clinical assessment of the visual fields showed

that central visual fields improved in 21 eyes, re-mained stable in 4, and worsened in 2, with no data for

the remaining 3 eyes; in the nonischemic hemi-CRVOgroup, the central field improved in two of three eyes

and remained stable in one eye. Our visual field eval-uation in both nonischemic CRVO and nonischemic

hemi-CRVO groups showed normal peripheral fieldsin all eyes initially as well as finally, except in six eyes

where segmental visual field loss (inferior nasal infour, superior altitudinal in one, and temporal sector in

one; Table 3) was the result of occlusion of a largecilioretinal artery, supplying a large segment of the

retina, that caused ischemic damage in that region and

resulted in peripheral visual field loss.

Anterior Segment

At the initial visit, findings of anterior segment

evaluation were within normal limits except for oneeye with ischemic CRVO that had iris neovascular-

ization. In the nonischemic CRVO group, the intraoc-ular pressure usually was 2 mmHg lower in the

involved eye (mean SD, 15.7 4.2 mmHg) than inthe fellow normal eye (17.9 6.8 mmHg), with a

marked difference in intraocular pressure between theinvolved eye and the fellow normal eye in a few

patients (e.g., 14 vs 51 mmHg in 1 eye, 16 vs 30

mmHg in 1, 12 vs 22 mmHg in 1, and 10 vs 16 mmHgin 1).

Vitreous

At the initial visit, there were some cells in thevitreous (a common finding in our studies on varioustypes of retinal vein occlusion): 12 eyes with nonisch-

emic CRVO, 2 with ischemic CRVO, and 1 withnonischemic hemi-CRVO. One of the eyes with non-

ischemic CRVO had asteroid hyalosis.

Optic Disk Changes

At the initial visit, the optic disk was edematous in

all eyes except 3 (2 eyes with nonischemic CRVO and1 with ischemic CRVO) and had hemorrhages on it

(22 with nonischemic CRVO, 3 with ischemic CRVO,and 2 with nonischemic hemi-CRVO); the severity of

disk edema varied from mild to marked. The opticdisk developed pallor (in the region of the retinal

infarct) in 20 eyes with nonischemic CRVO, 4 withischemic CRVO, and 2 with nonischemic hemi-

CRVO. Retinociliary collaterals were seen at clinicvisits 1.5 months to 10 months (mean SD, 5.2 3.0

month; median, 4.2 months) after onset in 9 eyes withnonischemic CRVO, after 4 months and 5.5 months in

2 with ischemic CRVO, and 3.5 months and 5 months

in 2 with nonischemic hemi-CRVO.

Table 3. Visual Field Defects at the Initial Visit

Type of VisualField Defect,No. of Eyes

NonischemicCRVO

IschemicCRVO

NonischemicHemi-CRVO

Total 30 5 3Central

scotoma

4 2 1

Centrocecalscotoma

13 3 0

Paracentralscotoma

4 0 1

Inferiorarcuatedefect

1 0 0

Inferiornasaldefect

4 0 1

Superioraltitudinaldefect

1 0 0

Temporalsectordefect

1 0 0

None 2 0 0

CRVO, central retinal vein occlusion.



6/14

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 theretinal 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 muchlarger 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 asector nasal to the optic disk in one.

The cilioretinal artery may or may not supply thefoveal 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), 0.5DD, 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 in2 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 onenonischemic hemi-CRVO eye, the infarct touched the

superior part of the fovea. When the foveal retina wasinvolved by the infarct, the part involved depended

upon the location of the cilioretinal artery, which may

run horizontally between the disk and the fovea orabove or below the horizontal line. When there was atiny or small cilioretinal artery, then it involved only

either the peripapillary retina or a small area adjacentbut away from the fovea. The retinal opacity caused

by infarction was usually more marked in the fovealregion, and at resolution, the opacity in that region

tended to be the last to resolve. We found that some ofthe tiny CLRAOs had been misdiagnosed ophthalmo-

scopically as cotton-wool spots. In a few eyes, therewas a white crescentlike opacity at the tip of the

cilioretinal artery supply, due to axoplasmic flow ob-

struction. Later on, the cilioretinal artery developedsheathing in some eyes.

Retinal Changes Due to CRVO or Hemi-CRVO

In all three groups of this study, apart from theretinal infarct caused by the CLRAO, the various

Table 4. Retinal Infarction Caused by Cilioretinal Artery Occlusion

Retinal Infarct, No. of EyesNonischemic

CRVO (n 30*)Ischemic


Hemi-CRVO (n 3)

Size of the occluded arteryLarge 6 0 1Medium 15 2 1Small 7 3 1Tiny 2 0 0

Foveal involvement by infractEntire fovea 2 1 0Upper half 2 0 0Superior nasal part 1 0 1No involvement 24 4 2

Infarct touchesFovea 4 2 1Foveola 2 0 0

Vertical height of infarct in disk diameters0.75 3 1 01 12 2 11.25 3 0 11.5 3 1 02 2 0 02.5 1 0 04.0 0 1 0Involves 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.



7/14

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 toretinal phlebitis at onset. At the final visit, perivenous

sheathing was seen in six eyes with nonischemic

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 thefoveal area in 6, 2, and 0 eyes, respectively, in the

macular region in 29, 5, and 3 eyes, respectively, andin 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 variousmacular changes seen at the initial visit and during

follow-up. When the CLRAO involved the centralmacular region, a cherry-red spot was seen. In a few

eyes seen early, swelling of the peripheral nasal fovealretina, associated with retinal infarction, caused lifting

up of the adjacent normal foveolar retina and visualacuity 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 0of 3 with nonischemic hemi-CRVO. These lesions

were mostly located in the temporal arcade regionsand, in some eyes, the peripapillary area.

Fluorescein Fundus Angiography Findings

Angiography was performed on all eyes in thisseries; 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 requiredfor evaluation of cilioretinal artery circulation were

unsatisfactory or missing because of poor cooperationfrom the patient. Angiographic findings were divided

into two categories.

Related to CLRAO.Relevant data related to

cilioretinal artery circulation by angiography in thisstudy 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 routineangiography. This showed that during the early stages

of the transit of the dye, the cilioretinal artery in theseeyes filled for a variable distance from the optic disk

during systole but the filling retracted to the optic diskduring diastole, resulting in an oscillating blood col-

umn in the cilioretinal artery, extending back and forthfrom the optic disk into the retina.

Fig. 1. Two examples showing the distribution and size of the retinalinfarct with cilioretinal artery occlusion in eyes with nonischemiccentral retinal vein occlusion. A, Infarct only in a narrow strip below

the foveola. B, Infarct involving most of the lower half of the retina.



8/14

Related to CRVO or Hemi-CRVO.These eyes also

had the well-known angiographic abnormalities seen

in eyes with CRVO or hemi-CRVO. The intervalbetween the start of filling of the retinal arteries and

that of the retinal veins (i.e., retinal arteriovenoustransit time) was very much prolonged: 7.7 3.6

seconds in nonischemic CRVO and 7.7 5.7 secondsin ischemic CRVO. During the late phase of angiog-

raphy, optic disk staining was most common, lesscommon than that was perivenous staining, and mac-

ular staining was least common.

Resolution of Retinopathy

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 3with nonischemic hemi-CRVO. In eyes where the reti-

nopathy resolved, it took a mean SD of 42.0 101.0months (median, 8.1 months; range, 0.7472.3 months)

in nonischemic CRVO and 15.4 4.5 months (median,15.4 months; range, 12.218.6 months) in ischemic

CRVO. The higher mean of the resolution time for the

Table 5. Macular Changes

Macular ChangeNonischemic CRVO

(n 30)Ischemic CRVO

(n 5)Nonischemic Hemi-CRVO

(n 3)

At initial visit*Edema and severity

Marked 0 3 0

Moderate 2 0 0Mild 5 0 2None 22 2 1

Foveolar cyst 5 3 1Later on during follow-upEpiretinal membrane 2 1 1RPE degeneration 3 1 0Cystoid degeneration 1 0 0

*One of 30 eyes was not seen during the acute phase.CRVO, central retinal vein occlusion; RPE, retinal pigment epithelium.

Table 6. Fluorescein Fundus Angiography Findings

FindingNonischemic

CRVO (n 30*)Ischemic


Hemi-CRVO (n 3)

Delayed filling of CLRAYes 20 3 2No 6 2 1No filling 2 0 0No data 2 0 0

Interval between central retinal artery and CLRA fillingNo filling 2 0 0Retrograde flow 2 0 0Delayed filling 17 2 1No delay 5 2 0No data 4 1 2

Total time it took for CLRA to fill completelyNo filling 2 0 0Delayed filling 20 2 2Normal 2 2 0No data 6 1 1

Capillary foveal arcadeIntact 25 0 3Broken 3 3 0No 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.



9/14

nonischemic type than for the ischemic type may be a

statistical artifact due to the low number of patients in thesubgroup.

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 ischemicCRVO) 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), incontrast 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 visualblurring before the onset of constant blurred vision

(Table 1). Only an occasional patient, of1,000 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 visualblurring before the onset of constant blurred vision

constitutes an important diagnostic feature of this clin-ical entity.

Deterioration of visual acuity in all three groupsmight have been due to either occlusion of the

cilioretinal artery per se, when it involved the fovealregion, 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 retinalinfarct involved the foveal zone, it resulted in perma-

nent central scotoma (Table 3). Overall visual acuityimprovement in the nonischemic CRVO group was

similar to that seen in eyes without any CLRAO,16 inspite of the associated CLRAO. It is important to point

out that when the infarct caused by CLRAO or abranch retinal artery touches the fovea (Fig. 1), ini-

tially visual acuity deterioration may simply be due toswelling of the foveal retina caused by the infarct,

which lifts up the adjacent normal foveolar retina; inthese eyes, visual acuity improves spontaneously

within a few weeks with resolution of the infarct,17

and that frequent spontaneous occurrence may be mis-

takenly attributed to various treatments.18 In contrast

to nonischemic CRVO, in ischemic CRVO, although4 (80%) of 5 eyes had no foveal involvement by the

CLRAO (Table 4), there was no similar visual acuityimprovement (Table 2); this was because foveal reti-

nal ganglion cells usually had irreversible ischemic

damage at the onset of ischemic CRVO, irrespectiveof foveal involvement by CLRAO. That basic differ-ence between ischemic and nonischemic CRVO was

responsible for the difference in visual acuity changeduring 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 dependupon the following: the size, location, and distribu-

tion of the occluded cilioretinal artery; the severityand 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 ofthe ischemic area may have already recovered visual

function by the time a patient is seen, leaving only acentral or paracentral scotoma instead of a centrocecal

scotoma. Like visual acuity, visual field improvementwas common in the nonischemic CRVO group, except

in eyes where an area of retina had had irreversibleischemic damage. Central visual fields improved in

70% of eyes with nonischemic CRVO. Peripheralvisual fields in both nonischemic CRVO and nonisch-

emic hemi-CRVO eyes were normal in all initially aswell as finally, except in six where segmental visual

field loss (Table 3) was the result of occlusion of alarge cilioretinal artery, supplying a large segment of

the retina.CRVO and hemi-CRVO usually cause a fall (2

mmHg) of intraocular pressure in the involved eye, bysome unknown mechanism. 19 There is a high preva-

lence of glaucoma or ocular hypertension amongCRVO and hemi-CRVO eyes. 19 In this study as well

as in our large CRVO study, we have seen that whenan 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 outglaucoma or ocular hypertension in the fellow unin-

volved eye.19 In view of that, treatment of ocularhypertension or glaucoma in the fellow eye is crucial

to reduce the risk of that eye developing CRVO orhemi-CRVO.



10/14

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 mayor may not involve the foveal region) (Table 4). The

ophthalmoscopic fundus findings due to CRVO, as

usual, consisted of engorged retinal vein, optic diskedema, retinal hemorrhages, and macular edema (Ta-ble 5). During follow-up, retinociliary collaterals de-

veloped in 30% (9 of 30) of eyes with nonischemicCRVO within 1.5 months to 10 months (median, 4.2

months) after onset, in 40% (2 of 5) of eyes withischemic CRVO within 4 months to 5.5 months of

onset, and in 66% (2 of 3) of eyes with nonischemichemi-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 eyesthe cilioretinal and central retinal arteries start to fill atthe same time. However, in eyes with CRVO associ-

ated with CLRAO, the filling pattern of the cilioretinalartery depends upon the time between the onset of

visual symptoms and fluorescein angiography. When

the eyes were seen shortly after the onset, they had aclassical oscillating blood column in the cilioretinal

artery (i.e., the artery filled for a variable distancefrom 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: theshorter the time interval (i.e., greater the retinal ve-

nous stasis), the longer it took the artery to fill. Table6 provides information about the delay in filling of the

cilioretinal artery when the patients were first seen inthe clinic, which in most cases was not at onset; this

delay in filling may be misinterpreted to mean that inour study the CLRAOs were most often not total. That

extent of delay depends upon the speed with whichthe venous collaterals developed in the optic nerve

and the time between the onset of visual symptomsand 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 duecourse in all eyes. In this study, during follow-up, the

retinopathy resolved in 73% (22 of 30) of eyes withnonischemic 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-upwas not long enough.

In our studies on CRVO, we have found that notevery eye with cilioretinal artery develops occlusion

and retinal infarct after CRVO. In our Ocular Vascular

Clinic, we have investigated CRVO and hemi-CRVOin a large cohort of patients since 1973. In a prelimi-

nary analysis of a cohort of the first 465 alphabeticallyconsecutive patients with CRVO (406 nonischemic

CRVO cases and 59 ischemic CRVO cases), we eval-

uated the eyes that had cilioretinal artery, but therewas no evidence of its occlusion, on the basis ofophthalmoscopic, angiographic, and visual field eval-

uations. Of the nonischemic CRVO eyes, 8% (32 of406) 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), mediumsized in 2, and large in 2 (in 1 eye, it supplied the

entire upper half of the retina). However, only 1 of 59eyes with ischemic CRVO without any occlusion had

a cilioretinal artery of small size.

Pathogenesis of Simultaneous Development ofCLRAO in Eyes With CRVO or Hemi-CRVO

Several hypotheses have been put forward to ex-

plain the simultaneous development of CLRAO andCRVO. McLeod and Ring4 postulated that in thesepatients, partial obstruction of their posterior ciliary

arteries may be the explanation for at least some of ourcases. 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 remainsunclear and the possibility of primary occlusion of the

cilioretinal artery must be considered in these eyes. It hasalso been proposed that optic disk edema caused by

CRVO can cause CLRAO. Some researchers have evenattributed 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 influencethe ocular blood flow. Blood flow in general depends

upon the intraluminal perfusion pressure (perfusionpressure arterial pressure venous pressure). There-

fore, factors that either reduce the arterial pressure orincrease 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 andvenous drainage systems of the retina between eyes

with an additional cilioretinal artery and eyes with thecentral retinal artery as the only source of blood sup-

ply. The venous drainage from the entire retina is bythe central retinal vein, irrespective of the numbers

and sources of the arteries that supply the retina. Ineyes with a cilioretinal artery, the arterial supply to



11/14

the retina is obviously from two independent sources:

the central retinal artery is the major source, and thecilioretinal 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 entireretina supplied by the cilioretinal arteries with nocentral 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 theretinal arterial bed caused by a rise in the retinal

venous pressure, the autoregulatory mechanism in theretinal arterial bed causes a rise in its pressure to try to

maintain retinal circulation. By contrast, because the

cilioretinal artery belongs to the choroidal vascularsystem, the following two entirely different mecha-nisms are working in the cilioretinal artery circulation

in eyes with CRVO: the choroidal vascular bed has noautoregulation in it, and there is no vortex venous

obstruction. Therefore, with sudden onset of CRVO, a

decrease in perfusion pressure in the central retinalartery kicks in the autoregulatory mechanism to main-

tain its blood flow; by contrast, no such compensatorymechanism exists in the cilioretinal artery. Moreover,

studies have shown that the perfusion pressure in thechoroidal vascular bed normally is lower than that in

the central retinal artery.2123

Thus, the theory that inthese eyes there is partial obstruction of their posterior

ciliary arteries and that this represents a spectrum ofocular vascular lesions intermediate between acute

central retinal vein occlusion and acute ischemic opticneuropathy4 is not valid; moreover, there is no evi-

dence of anterior ischemic optic neuropathy in theseeyes.

In the light of the above-mentioned facts, let us lookat 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 capillarybed; when that intraluminal pressure rises above that

in the cilioretinal artery, the result is a hemodynamicblock in the cilioretinal artery. For many of these eyes,

angiography performed during the early acute phaseprovided information about the in vivo dynamics of

blood flow in the eye. During the early stages of thetransit of the dye, the cilioretinal artery in these eyes

usually filled up to the optic disk, because the opticnerve head is supplied mainly by the posterior ciliary

arterial circulation.24,25 During systole, the cilioretinalartery often filled for a variable length from the optic

disk into the retina, but during diastole, the filling

retracted to the optic disk, resulting in an oscillatingblood column in the cilioretinal artery, moving back

and forth from the optic disk for a variable distanceinto the retina. Thus, the CLRAO in these eye is

simply a hemodynamic block and not due to embolism

or thrombosis. The hemodynamic block is invariablytransient, lasting from a few hours to several days,depending upon how rapidly the collateral circulation

is established by the central retinal vein through itsmultiple 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, thereis 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 circulationin the distribution of the cilioretinal artery. Hence, if apatient with CRVO is seen for the first time many days

after the onset of CLRAO, a retinal infarct is presentophthalmoscopically, 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 twotrunks 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 firstdiscovered 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 pressuremonitoring for 700 patients, for whom blood pres-

sure was recorded every 10 minutes during the wakinghours and every 20 minutes during sleep. In our stud-

ies,26,27 we found that during sleep there is a fall ofsystolic blood pressure by 34.8 1.2% and a fall of

diastolic blood pressure by 44.0 1.3% from daytimeblood pressures.27 This fall of blood pressure is ag-

gravated by overmedication with blood pressurelow-ering medication, particularly when the medication is

given in the evening or at bedtime. There were twoother important relevant findings of our study. The



12/14

most impressive finding of our 24-hour ambulatoryblood pressure monitoring study was that systemic

arterial blood pressure is the most volatile parameterin the human body and is greatly influenced instanta-

neously by physical or emotional factors. Daytimeblood 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 apatient who has just had visual loss and is emotionally

upset. In view of that, arterial hypertension discoveredin 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 transientarterial hypertension in his ophthalmologists office

may be treated aggressively by physicians withoutrealizing 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 hasimportant implications both for comprehension of the

mechanism of development of CLRAO with CRVOand for management of these patients (see below).

Therefore, in eyes with CRVO and cilioretinal ar-tery, the following sequence of events takes place: fall

of systemic blood pressure during the night, secondary

falls in the cilioretinal artery blood pressure (withoutany 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 beforethe onset of constant blurred vision (Table 1). This is

most probably also due to a transient fall in systemicblood pressure during waking hours, for whatever

reason (e.g., orthostatic hypotension), resulting in atransient hemodynamic block in the cilioretinal artery.

Naturally, the following question arises: Why did onlyone third of the patients have transient vision blurring

before the onset of constant blurred vision and not allpatients? Whether a patient gets these episodes of

transient blurring before developing CLRAO dependsupon the difference between the intraluminal pressure

in the retinal capillary bed and that in the cilioretinalartery (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

Fig. 2. Ambulatory bloodpressure (top) and heart rate(bottom) monitoring record

(based on individual read-ings) staring at 11 AM and go-

ing on until 10 AM the nextday.



13/14

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 weeksafter the onset of visual blurring, had no evidence ofinfarction 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 arteryfilling. This may be due to slow development of

CRVO, which allows time for collaterals to develop inthe optic nerve, so that the intraluminal pressure in the

retinal capillaries never gets high enough to causehemodynamic block in the cilioretinal artery. The

other possible explanation is that the cilioretinal artery

is a direct branch of the posterior ciliary artery20

andis not a part of the choroidal vascular bed, so that it hasthe 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 visualobscuration, 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 theretinal capillary bed is high enough to cause delayed

filling of the cilioretinal artery, it is not high enough toproduce a complete hemodynamic block and infarc-

tion yet is high enough to produce transient visualobscuration. This would indicate that delayed filling

of the cilioretinal artery is present much earlier thandevelopment of complete hemodynamic block and

retinal infarction. Most likely, the retinal infarctiondevelops in these eyes when nocturnal arterial hypo-

tension during sleep causes intraluminal pressure inthe cilioretinal artery to fall below the critical level,

resulting in a hemodynamic block in the cilioretinalartery that lasts many hours.

In two eyes in the present series, there was onlynonischemic CRVO at the initial visit, but at the next

follow-up visit, they were found to have developedCLRAO some time during the intervening period,

indicating that CLRAO can occasionally develop lateron. 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 onwaking in the morning.

From the management point of view, for patientswho present with any of the above-mentioned symp-

toms or findings, it is essential to evaluate and regulate

their blood pressurelowering medication, to preventfurther visual loss. Our 24-hour ambulatory blood

pressure monitoring studies have shown that patientswho are overmedicated with blood pressurelowering

drugs or take those drugs in the evening or at bedtime

are highly susceptible to develop marked nocturnalarterial hypotension27 and consequent visual loss.

To understand why some eyes with CRVO associ-

ated with CLRAO develop permanent visual loss inthe distribution of cilioretinal artery while others have

only temporary loss, it is essential to consider retinaltolerance time to acute ischemia. Our studies have

shown that acute retinal ischemia lasting for up to100 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 ofvisual function.28,29 Therefore, in eyes with CRVOassociated with CLRAO, the severity of visual loss

and the recovery of retinal function depend upon theduration 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 includes38 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 thisstudy may be considered by some a limitation; how-

ever, it roughly coincides with their overall incidencein 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, retinalartery, retinal vein.

References

1. Oosterhuis JA. Fluorescein fundus angiography in retinal ve-nous occlusion. In: Henkes HE, ed. Perspective in Ophthalmol-

ogy. Amsterdam: Excerpta Medica Foundation; 1968:2947.

2. Hayreh SS. Pathogenesis of occlusion of the central retinal

vessels. Am J Ophthalmol 1971;72:998l011.

3. McLeod D. Cilio-retinal arterial circulation in central retinal

vein occlusion. Br J Ophthalmol 1975;59:486492.

4. McLeod D, Ring CP. Cilio-retinal infarction after retinal vein

occlusion. Br J Ophthalmol 1976;60:419427.

5. Glacet-Bernard A, Gaudric A, Touboul C, Coscas G. Occlu-

sion de la veine centrale de la retine avec occlusion dune

artere cilio-retinienne: a propos de 7 cas. [Occlusion of the

central retinal vein with occlusion of a cilioretinal artery: a

propos of 7 cases.] J Fr Ophtalmol 1987;10:269277.



14/14

6. Schatz H, Fong ACO, McDonald HR, et al. Cilioretinal artery

occlusion in young adults with central retinal vein occlusion.

Ophthalmology 1991;98:594601.

7. Brazitikos PD, Pournaras CJ, Baumgartner A. Occlusion

dune artere cilioretinienne associee a une occlusion de la

veine centrale de la retine. [Occlusion of a cilioretinal artery

associated with occlusion of the central retinal vein.] Klin

Monatsbl Augenheilkd 1991;198:374376.8. Keyser BJ, Duker JS, Brown GC, et al. Combined central

retinal vein occlusion and cilioretinal artery occlusion asso-

ciated with prolonged retinal arterial filling. Am J Ophthal-

mol 1994;117:308313.

9. Browning DJ. Patchy ischemic retinal whitening in acute central

retinal vein occlusion. Ophthalmology 2002;109:21542159.

10. Hayreh SS, Hayreh MS. Hemi-central retinal vein occlusion.

Pathogenesis, clinical features, and natural history. Arch

Ophthalmol 1980;98:16001609.

11. Hayreh SS. Classification of central retinal vein occlusion.

Ophthalmology 1983;90:458474.

12. Hayreh SS, Klugman MR, Beri M, et al. Differentiation of

ischemic from non-ischemic central retinal vein occlusion

during the early acute phase. Graefes Arch Clin Exp Oph-

thalmol 1990;228:201217.13. Hayreh SS, Klugman MR, Podhajsky P, et al. Argon laser

panretinal photocoagulation in ischemic central retinal vein

occlusiona 10-year prospective study. Graefes Arch Clin

Exp Ophthalmol 1990;228:281296.

14. Hayreh SS. Posterior ischaemic optic neuropathy: clinical

features, pathogenesis and management. Eye 2004;18:1188

1206.

15. Hayreh SS, Zimmerman MB. Central retinal artery occlusion:

visual outcome. Am J Ophthalmol 2005;140:376391.

16. Hayreh SS. Management of central retinal vein occlusion.

Retina 2007;27:514517.

17. Hayreh SS. Prevalent misconceptions about acute retinal

vascular occlusive disorders. Prog Retin Eye Res 2005;24:

493519.

18. Hayreh SS. Surgical removal of retinal artery occlusion. Br J

Ophthalmol 2007;91:10961097.

19. Hayreh SS, Zimmerman MB, Beri M, Podhajsky P. Intraoc-

ular pressure abnormalities associated with central and hemi-

central retinal vein occlusion. Ophthalmology 2004;111:133

141.

20. Hayreh SS. The cilio-retinal arteries. Br J Ophthalmol 1963;

47:7189.

21. Hayreh SS. Pathogenesis of visual field defectsrole of the

ciliary circulation. Br J Ophthalmol 1970;54:289311.22. Hayreh SS, Revie HIS, Edwards J. Vasogenic origin of visual

field defects and optic nerve changes in glaucoma. Br J

Ophthalmol 1970;54:461472.

23. Blumenthal M, Best M, Galin M, Gitter KA. Ocular circula-

tion: analysis of the effect of induced ocular hypertension on

retinal and choroidal blood flow in man. Am J Ophthalmol

1966;75:806807.

24. Hayreh SS. Blood supply of the optic nerve head and its role

in optic atrophy, glaucoma and oedema of the optic disc. Br

J Ophthalmol 1969;53:72l748.

25. Hayreh SS. The blood supply of the optic nerve head and the

evaluation of itmyth and reality. Prog Retin Eye Res 2001;

20:563593.

26. Hayreh SS, Zimmerman MB, Podhajsky P, Alward WLM.

Nocturnal arterial hypotension and its role in optic nerve headand ocular ischemic disorders. Am J Ophthalmol 1994;117:

603624.

27. Hayreh SS, Podhajsky PA, Zimmerman B. Role of nocturnal

arterial hypotension in optic nerve head ischemic disorders.

Ophthalmologica 1999;213:7696.

28. Hayreh SS, Zimmerman MB, Kimura A, Sanon A. Central

retinal artery occlusion. Retinal survival time. Exp Eye Res

2004;78:723736.

29. Hayreh SS, Jonas JB. Optic disk and retinal nerve fiber layer

damage after transient central retinal artery occlusion: an

experimental study in rhesus monkeys. Am J Ophthalmol

2000;129:786795.

30. Hayreh SS, Zimmerman MB, Podhajsky P. Incidence of

various types of retinal vein occlusion and their recurrence

and demographic characteristics. Am J Ophthalmol 1994;

117:429441.


OVCR combinado OACR

Documents

Transcript of OVCR combinado OACR