TABLE 1.
Stage No.
Reprinted with permission from Archives of Ophthalmology
(1987;105:906-912).
Reprint requests to (J.T.F.) Bascom Palmer Eye Institute, P0 Box 016880, Miami, FL 33101.
An International
Classification
of Retinopathy
of
Prematurity
II. The
Classification
of Retinal
Detachment
From the International Committee for the Classification of the Late Stages of Retinopathy of Prematurity
The purpose of this article is to complete the
classification ofretinopathy ofprematunity (ROP)
begun with the publication of the recent article
on the subject entitled, “An International
Clas-sification of Retinopathy of Prematurity”
(ICROP).’3 The previously published
classifica-tion embodied three major concepts for the
de-scniption of the early phases of the disease:
spec-ifying its location by zones ofretinal involvement;
recording the extent of retinal involvement by
clock hours; and, finally, staging the disease
ac-cording to the degree of vascular lesions observed
(stages 1 through 4). That article specified
pos-tenor dilatation and tortuosity of retinal vessels
as ominous prognostic signs. The committee that
authored it left unclassified the sequelae that
en-compass the cicatnicial phase ofthe disease. It
nec-ommended the use of the Reese classification4
until a more satisfactory one could be developed.
The reasons for completing the classification of
the end stages ofROP at this time are compelling.
First, there has been an increase in the survival
rate of infants of low birth weight who are most
likely to develop the severe forms of the disease.
Second, surgical treatment of these blind or
near-blind infants is being undertaken without
know-ing which stage is being treated and what the
im-plications of the results of such treatment are.
Fi-nally, as a result of further surgical observations
and study of pathologic specimens, we now have
an increased understanding ofthe development of
the severe end stages of ROP.
THE CLASSI
FICATION
The system presented herein elaborates the
fea-tures of the retinal detachment (stage 4) of the
international classification. It eliminates the
term cicatricial and reaffirms a commitment to the term retinopathy ofprematurity for all stages
and manifestations of the disease. The reason for
this is that the major cause of visual loss and
blindness in ROP is the traction detachment of
the retina that often has exudative features.
Then-apeutic efforts of any type must be aimed at
pre-venting and repairing this detachment. The
clas-sification leaves intact the previous parameters,
location, and extent specified in ICROP. The focus
of its description is on the morphology, location,
and extent ofthe retinal detachment. To that end,
stage 4 of ICROP has been expanded, and a fifth
stage has been added to the classification itself
(Table 1).
Each of these additions deserves explanatory
comment.
Stage
4A
Extrafoveal retinal detachment (Fig 1) is a
con-cave, traction type of detachment that occurs in
the periphery without involvement ofthe macula.
The prognosis for vision, in the absence of
exten-sion posteriorly, is relatively good. Generally,
Stage of Retinopathy of Prematurity
Characteristic
1 Demarcation line
2 Ridge
3 Ridge with extraretinal fibrovascular
proliferation
4 Subtotal retinal detachment
A. Extrafoveal
B. Retinal detachment including fovea
5 Total retinal detachment
Funnel: Anterior Posterior
Open Open
Narrow Narrow
Open Narrow
TABLE
2. Regressed Retinopathy of PrematurityPeripheral Changes
Vascular
1. Failure to vascularize peripheral retina
2. Abnormal, nondichotomous branching of retinal vessels
3. Vascular arcades with circumferential interconnection
4. Telangiectatic vessels Retinal
1. Pigmentary changes
2. Vitreoretinal interface changes
3. Thin retina 4. Peripheral folds
5. Vitreous membranes with or without attachment to ret-ma
6. Latticelike degeneration
7. Retinal breaks
8. TractionJrhegmatogenous retinal detachment
Posterior Changes
Vascular
1. Vascular tortuosity
2. Straightening of blood vessels in temporal arcade 3. Decrease in angle of insertion of major temporal arcade Retinal
1. Pigmentary changes
2. Distortion and ectopia of macula
3. Stretching and folding ofretina in macular region leading to periphery
4. Vitreoretinal interface changes 5. Vitreous membrane
6. Dragging of retina over disc
7. Traction/rhegmatogenous retinal detachment
these detachments are located in anterior zone II
or zone III. They may be circumferential, in which
case they extend for 360#{176},or segmental, occupying
only a portion of the circumference of the
periphery.
Stage
4
Partial retinal detachment including the fovea
(Fig 2) is segmental and usually extends in the
form of a fold from the disc through zone I to
in-volve zone II and zone III. The prognosis for vision
in this second segmental type of subtotal retinal
detachment is poor.
Stage
5
Total retinal detachment (Fig 3) is always
fun-nel shaped. The configuration of the funnel itself
permits a subdivision ofthis stage. For descriptive
purposes, the committee divided the funnel into
an anterior and a posterior part. When open both
anteriorly and posteriorly, the detachment has a concave configuration and extends to the optic
disc (Fig 4). A second frequent configuration is one
in which the funnel is narrow in both its anterior
and posterior aspects and the detached retina is
located just behind the lens (Fig 5). A third less
common type is one in which the funnel is open
anteriorly but narrowed posteriorly. Least
com-Fig 1. Top, Artist’s sketch of stage 4: subtotal retinal
detachment that remains outside fovea. Original ridge
at site of early retinopathy of prematurity is seen on
surface of detached retina. Center, Gross specimen
shows buckling and localized detachment of temporal
postequatonial retina with conspicuous extraretinal
vascularization. In addition to large vessels (large
arrow) and small vessels (small arrow), overlying
vit-reous shows degenerative changes ( x 7.5). Bottom,
His-tologic section confirms these features and shows focus
of hemorrhage in vitreous anteriorly (arrow)
(hema-toxylin-eosin, x 63).
Fig 2. Top, Artist’s sketch of stage 4: subtotal retinal
detachment including fovea. Detachment involves
fovea and optic disc. Vessel architecture in posterior
pole is severely stretched. Bottom, Fundus photograph
of detached retina extending through macula to optic
disc.
Fig 3. Top, Artist’s sketch of stage 5: total retinal
de-tachment extending posteriorly in narrow funnel to
optic disc. Note peripheral trough (arrows). Bottom,
Photograph ofinfant’s eye with funnel-shaped total
ret-inal detachment.
Fig 4. Top, Gross specimen shows folding and scroll-like rolling of peripheral retina with foreshortening
and detachment of entire retina posteriorly. Vitreous
shows severe synchysis centrally and is condensed
be-hind lens and on detached retina posteriorly ( x 4.6).
Bottom, Histologic section of similar specimen shows
folding and rolling of peripheral retina (at site of
extraretinal vascularization) and total detachment of
foreshortened retina (open funnel configuration)
(hematoxylin-eosin, x 5).
Fig 5. Top, Gross specimen shows folding and rolling of peripheral retina and total detachment of posterior
retina. Funnel of detached retina is extremely narrow
posteriorly and closed anteriorly with retrolental
fi-brous plaque. Arrow shows trough formed by
periph-era! retina and ciliary epithelium ( x 4.6). Bottom,
His-tologic section of similar specimen shows narrow
funnel-shaped total retinal detachment
(hematoxylin-eosin, x3.6).
Fig 6. Peripheral fundus photograph showing paucity
of retinal vessels and area of avascular retina (arrow)
anterior to equator with regressed retinopathy of
prematurity.
Fig 7. Abnormal vessel formation in periphery with
vascular arcades and shunt vessels (arrow) in region of
regressed retinopathy of prematurity.
mon is a funnel that is narrow anteriorly and open
posteriorly. These more unusual configurations of
the funnel-shaped detachment of stage 5 ROP can
Fig 1.
Fig 5.
Fig 4.
I
;‘ ,
U‘L Subtle pe J pigmentary
changes seen commonly in areas of
major involvement in retinopathy of
prematurity.
F
,, . Large plaque of retinalpig-ment epithelial change with exudates in periphery in regressed retinopathy
of prematurity. Fig 1 0. Retinovitreous interface
changes (arrow) in fundus periphery
that take form of delicate line in area
of previously active retinopathy of
prematurity.
changes (arrow) in regressed
retino-pathy of prematurity with more
marked distortion of vessel and
reti-nal architecture.
41
. #{149}_./
,.,,“
Fig 12. Distortion of macula due to
traction in regressed retinopathy of
prematurity.
Fig 1 4. Totally detached retina
lo-cated behind lens, covered with
trans-lucent membrane containing retinal
blood vessels.
Fig I 5. Avascular membrane
coy-ening surface of totally detached ret-ma in retrolenticular space.
Fig 1 6. Oblique photograph of
pe-ripheral trough seen in partial
de-tachments of retina with severe
stretching of avascular retina that
nevertheless remains attached.
Fig 1 7. Anterior segment of infant’s
eye with stage 5 retinopathy of
pre-maturity showing shallow anterior
chamber, iris blood vessel, and poor
dilatation of pupil.
Fig I 3. Severe distortion of retina
and vessel architecture in posterior
pole in regressed retinopathy of
22
ZI Zil ZIlI
11-12 Ti 12-1
10-11 tt1 1-2
9-10 2-3
8-9 lt1
7-8
ti
4-56-7 5-6
Date of cse I I Fcaminer’s Initials or *
o.s.
- ZI Zil ZIII
11-12 IT) 12-1
10-11
I11
1-29-10 M1 2-3
8-9 3-4
7-B I I I 4-5
6-7 5-6 0.0. 0.0. 0.S. 0. S. 0.D. 0.5. Retinal - Pige.ntary
- Distortmon/ectopia of treculs
- Fold of retina
- V-R interface changes
- Vitreous ranes
- Dragging of retina over disc
TractioiVrhesstogenoua
- retinal detacheent
0.5.
Retinal
- Pigeantary changes
- V-R interface changes
Thin retioa - Peripheral folds
- Vitreous smabranes
REFDIOPAThY OF PR4AIT( (ROP) OPIfNALI4IC FXN4INTI1 RR II
BICAPIiICAL DATh
Ni______________________ Hospital I
Birthdate (141/DO/YY) I I Sex (14-1, F-2)
Birthight (gr) _ _ __ _ Geatational qe (eks)
tt1tip1e Births (Single-i, Twin-2, Triplet-3)
NflI Sfl’
(0 - no information, 1- yes, 2- rc)
1. Cornea
Clear
Cloudy
2. Anterior chnber
Nonal depth Shall Absent 3. Iris Normal Active vasculature Atrophy Synechise 4. Pupil Nozmal Fixed Secl S. Lens Clear Cataract
6. Retrolental space
Clear Vascularized eaitrane 7. Vitreous Clear Nsnorrhage RSa
(0 - no information, 1- Present, 2- Absent)
A. Peripheral thanges
Vascular
0.0.
- Failure to vascularize to ora
- Abnormal branching
- Vascular arrmdes
- langiectatic vessels
0- No vim possible
1- na.rcation line
2- Ridge
3- Ridge plus estraretinal proliferation
4- Stage 4A, subtotal R.D. without nmcula detactsmnt
5- Stage 45, subtotal R.0. with cula detadieant
6- Stage 5, total detactient, open funnel
7- Stage 5, tOtal dstactsvent, nerr funnel
8- Stage 5. type undetermined
9- Avascular, retina attached
Other Findings
If Stage 3: 0-no info, lnild, 2ierate, 3-severe
Dilatation/tortuosity posterior vessels:
0-no information, 1-yes, 2-no
PenJRE OF o#{128}r:*iwr
1. Type of detactinent present
0- no information
1- none
2- traction 3- exudative
4- cained 5- rhegsatcgenous
2. Macala
0- no information
1- attached
2- shall detactsent
3- high detactsnent
3. Peripheral Trc*4:
1- not visible
2- present
4. Subretinal fluid
0- no information
1- clear 2- blcx,dy 3- exudate
B. Posterior thanges
Vascular
0.0. 0.S.
- ‘Ibrtuosity
-- Straightening of vessels
tcrease in angle of insertion
- of jor te#{231}oral arcmde
REGRESSED
ROP
Though not, strictly speaking, an integral part
of the classification, the committee recognizes
that regression is the most common outcome of
ROP. Regression has a broad spectrum of
peniph-era! and posterior retinal and vascular changes
that are tabulated in Table 2. Such a wide variety
of changes may be encountered in regression that
classifying them is almost impossible. Thus, it is
recommended that these changes be recorded on
the appropriate form when they are encountered
(vide infra).
The common thread underlying the changes of
regression is the notion that the more severe the
original disease in its location, extent, and
de-velopment through the stages, the more serious
the changes left behind by the process when it
regresses. Vascular abnormalities such as
prom-inent areas of retina! avasculanity (Fig 6),
abnor-ma! branching of vessels with formation of
an-cades (Fig 7), and telangiectatic vessels would be
expected to be conspicuous features. Pigmentary
changes may be subtle (Fig 8) but more often
be-come large areas located along blood vessels and
in underlying pigment epithelium, as seen
through an avascular retina (Fig 9).
Circumfer-ential retinovitreous interface changes may be
seen as delicate lines (Fig 10) or more prominent
ridges (Fig 1 1). The more severe the peripheral
changes, the more severe the posterior pole
changes. These can vary from minor distortions
of fovea! architecture (Fig 12) to severe
displace-ments of the major retinal vessels, usually
tem-porally and often accompanied by dragging of the
retina oven the disc (Fig 13). Finally, traction and
rhegmatogenous retinal detachment and, rarely,
exudative detachment can develop as late
com-plications of regressed ROP.
OTHER
FACTORS
The committee feels that attention should be
drawn to certain physical findings observable in
stages 4 and 5 of ROP.
1.
The appearance of the netnolenticulan space:This space may be occupied by heavily
vascular-ized translucent tissue (Fig 14), which represents
a more active phase of the disease. The tissue
oc-cupying this space may be white with a paucity
of blood vessels (Fig 15).
2. Peripheral trough: The presence of a
pe-ripheral ned reflex in combination with what
ap-pears to be a narrow-funnel stage 5 retinal
de-tachment indicates the presence of attached or
shallowly detached avascular, stretched, and
non-functioning peripheral retina (Fig 16).
3. Anterior segment: Though not involving
pni-manly the anterior segment of the eye, the more
severe stages of retinopathy of prematurity do
have important consequences for its structure and
integrity. The changes in the anterior segment
can be described as follows.
(a) Shallow anterior chamber and cornea!
edema: A shallow anterior chamber may be a
nor-ma! early finding in a premature infant’s eye;
however, when a shallow anterior chamber
de-velops along with a retinal detachment in ROP,
it has more serious significance (Fig 17). When
accompanied by cornea! edema, it is often due
to elevated intraocular pressure but may also
occur in hypotonous eyes. These changes are seen
most commonly in the most severe form of stage
5 ROP.
(b) Iris atrophy, posterior synechiae and
ectro-pion uveae: During the course of ROP, the iris
may become rigid and the pupil may become
dif-ficu!t to dilate. Adhesions to the anterior lens
cap-sule, persistence of the pupi!lary membrane with
retention of its vascular network, and migration
of the iris pigment epithelium onto the anterior
surface of the iris occur.
(c) Other tissues: In addition to the retinal
de-tachment, other findings may be present that
have prognostic significance for the eye.
Subre-tina! blood and exudate may be identifiable by
ultrasonographic examination but can be difficult
to distinguish from one another by this modality.
Subretina! membranes may be present, but they
are usually recognized only during surgery.
RECORDING
THE RESULTS
As in the previous classification, a
computer-compatible examination record for detailing the
ophthalmic examination results has been
devel-oped (Fig 18). With the completion of the
classi-fication of retina! detachment, this replaces the
section “Cicatnicial Disease” on the previously
published form. Should the disease be amenable
to surgical therapy, the examination record may
be adapted to permit preoperative, intraoperative,
and postoperative recording of observations on a
single form.
COMMENT
No classification scheme is perfect. The purpose
of this one is to describe the morphology of the
retinal detachment in the clearest terms possible.
In so doing, the classification has focused
pni-manly on the detachment itself. These changes
represent the final stage of a very complex
under-stood. Obviously, such a strategy involves
aban-doning the time-honored divisions of the Reese
classifications into acute and cicatnicial as well as
the estimated visual acuity values assigned for
each grade of cicatnicial disease. We chose to
rep-resent the morphology of the retinal detachment,
specifying its location and extent in terms of the
zone and clock-hour concept employed in our
in-itial article. In so doing, we hope to unite under
one heading an understanding, as fan as is
pos-sible, of all aspects of ROP that result in severe
visual loss in the infant. The changes of regressed
ROP are the most common sequelae but, since
they can occur at almost any stage before
detach-ment, they are not recorded as a distinct stage in
the main classification. It is recognized that these
changes may be of long-term significance to the
eye and may lead to complications such as myopia,
anisometropia, strabismus, and amblyopia and,
therefore, need documentation and follow-up over
the years. Provision for this is made on the
ex-amination record.
SPONSORSHIP
This classification is the product of the joint
ef-forts of 21 ophthalmologists and pathologists from
seven countries. Though an ad hoc body, we
ob-tamed sponsorship for our deliberations from the
American Academy of Ophthalmology, American
Academy of Pediatrics, American Association of
Pediatric Ophthalmology and Strabismus,
Divi-sion of Maternal and Child Health of the Bureau
of Health Care Delivery and Assistance, The
Na-tional Eye Institute, March ofDimes, The Macula
Foundation, National Children’s Eye Care
Foun-dation, The Macula Society, the Retina Society,
the Vitreous Society and the Gonin Society. As in
the previous study, these organizations have
pro-vided encouragement and support that, in no
small measure, enabled the committee to
com-plete this classification. The success or failure of
the classification itself will be judged by its use
within the ophthalmo!ogica! and pediatric
com-munities throughout the world.
ACKNOWLEDGMENTS
This study was supported in part by Public Health Service research grant EYO3513, National Institutes
of Health; US Department of Health and Human
Ser-vices, Public Health Services Division of Maternal and
Child Health, Bethesda, Md; The March ofDimes Birth
Defects Foundation, White Plains, NY; The Macula
Society; The Macula Foundation; The National
Chil-dren’s Eye Care Foundation; The Retina Society; The
Vitreous Society; and The Gonin Society.
Illustrations by Allison Medical Illustrators Inc (Eric
Grafman, MS, Barbara Cousins, and Leona M. Allison,
MS).
REFERENCES
COMMIVFEE MEMBERS
Thomas Aaberg, MD, United States
Isaac Ben-Sira, MD, Israel
Steve Charles, MD, United States
John C!arkson, MD, United States
Ben Zane Cohen, MD, United States
John Flynn, MD, United States
Robert Foos, MD, United States
Alec Garner, MD, PhD, Great Britain
Tatsuo Hirose, MD, United States
Fritz Koerner, MD, Switzerland
Robert Machemer, MD, United States
Akio Majima, MD, Japan
Andrew McCormick, MD, Canada
Alice McPherson, MD, United States
He!ge Pau!mann, MD, West Germany
Graham Quinn, MD, United States
Joseph Robertson, MD, United States
Yasuhiko Tanaka, MD, Japan
William Tasman, MD, United States
Tnexler Topping, MD, United States
Michael Trese, MD, United States
1. Committee for the Classification of Retinopathy of
Pre-maturity: The International Classification of Retinopathy of Prematurity. Arch Ophthalmol 1984;102: 1130-1134 2. Commmittee for the Classification of Retinopathy of
Pre-maturity: The International Classification of Retinopathy
of Prematurity. Pediatrics 1984;74:127-133
3. Committee for the Classification of Retinopathy of Pre-maturity: The International Classification of Retinopathy of Prematurity. Br J Ophthalmol 1984;68:690-697
4. Reese AB, King M,J, Owens WC: A classification of
