Outcome of retinopathy of prematurity patients following adoption of revised indications for treatment

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BMC Ophthalmology
Open Access
Research article
Outcome of retinopathy of prematurity patients following adoption
of revised indications for treatment
Aaron M Alme, Michael L Mulhern, Thomas W Hejkal, Jane L Meza,
Fang Qiu, David D Ingvoldstad and Eyal Margalit*
Address: University of Nebraska Medical Center, Department of Ophthalmology and Visual Sciences, Omaha, Nebraska, USA
Email: Aaron M Alme - aalme@unmc.edu; Michael L Mulhern - mmulhern@unmc.edu; Thomas W Hejkal - twhejkal@unmc.edu;
Jane L Meza - jmeza@unmc.edu; Fang Qiu - fqiu@unmc.edu; David D Ingvoldstad - dingvold@gmail.com;
Eyal Margalit* - emargalit@unmc.edu
* Corresponding author
Abstract
Background: The Early Treatment for Retinopathy of Prematurity study (ETROP), published in
2003, established new guidelines for treatment of retinopathy of prematurity (ROP) and
demonstrated improved outcomes compared to previous guidelines. We examined outcomes
before and after implementing the ETROP recommendations.
Methods: A retrospective chart review was performed using records of infants who had laser
ablations for ROP performed from January, 2000 through December, 2005. Data collected included
date of birth; birth weight; estimated gestational age (EGA); grading of ROP; date of laser ablation;
and outcome of laser surgery. Univariate association with threshold or prethreshold treatment
(Pre-ETROP and Post-ETROP, respectively) were assessed using t-tests or Wilcoxon tests.
Additional comparison between groups was performed using Fisher's exact tests.
Results: 581 patients were examined before and 464 after December 2003. Of these, 29/581 (5%
– Pre-ETROP Group) and 53/464 (11% – Post-ETROP Group) patients advanced to criteria
requiring laser treatment respectively (P = 0.0001). The average estimated gestational age (EGA)
at birth was 26.3 and 25.2 weeks, with an average birth weight of 888 and 707 grams for Pre and
Post-ETROP Groups, respectively. Stage 5 retinal detachment (RD) developed in 10.3% of eyes in
the Pre-ETROP Group and 1.9% of eyes in the Post-ETROP Group (P = 0.02).
Conclusion: After the ETROP guidelines were implemented, there was a decrease from 10.3% to
1.9% of eyes developing Stage 5 retinal detachment, despite this group having a lower average EGA
and lower average birth weight. These results underscore the importance of adoption of the
Revised Indications.
Background
Retinopathy of prematurity (ROP) is a proliferative vascu-
lar retinopathy affecting infants of young gestational age
and low birth weight. First described by Terry in 1942,
ROP remains a leading cause of lifelong visual impair-
ment among premature children in developed countries
[1-11].
Published: 13 November 2008
BMC Ophthalmology 2008, 8:23doi:10.1186/1471-2415-8-23
Received: 5 March 2008
Accepted: 13 November 2008
This article is available from: http://www.biomedcentral.com/1471-2415/8/23
© 2008 Alme et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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The multi-center trial of Cryotherapy for Retinopathy of
Prematurity (CRYO-ROP) showed that 44.4% of eyes with
a history of severe ROP had a visual acuity at age 10 years
of 20/200 or worse. Of those children with visual acuities
better than 20/200, only 45.4% had a visual acuity of 20/
40 or better [2,3]. This prompted investigators to pursue
more effective approaches to treatment.
In the CRYO-ROP study, peripheral retinal ablation were
performed in eyes when the severity of ROP reached a
point at which the risk of progression to RD was approxi-
mately 50%; this was termed threshold ROP [4-8,11].
Threshold ROP was defined as 5 contiguous or 8 non-con-
tiguous clock hours of stage 3 ROP in zone I or II in the
presence of plus disease. While some surgeons expressed
concern regarding the treatment risks of earlier interven-
tion, others strongly advocated earlier treatment despite
the possibility that the ROP in many of these patients may
regress spontaneously.
The National Eye Institute in 1999 sponsored a multi-
center study of early treatment for ROP (ETROP study).[8]
Eyes of infants were randomized to a) standard manage-
ment based on CRYO-ROP recommendations, or b) early
peripheral retinal ablation, if they developed prethreshold
ROP. Prethreshold ROP was defined as:
▪ Zone I, any stage ROP that was less than thresh-
old
▪ Zone II, Stage 2 ROP with plus disease
▪ Zone II, Stage 3 ROP without plus disease
▪ Zone II, Stage 3 ROP with plus disease but
fewer than 5 contiguous or 8 cumulative clock hours of
neovascularization [8].
The ETROP data, published in December 2003, demon-
strated a benefit of earlier treatment compared with con-
ventional management, with regard to both structural
outcome and grated visual acuity [8]. In the ETROP study,
all infants < 1251 g were screened. Initial screening is gen-
erally recommended for infants with a birth weight of <
1500 grams or with a gestational age of 30 weeks or less.
Our research aim was to compare outcomes of infants
with ROP managed according to the CRYO-ROP guide-
lines to those managed under the ETROP guidelines. The
demographics of treated patients were also evaluated.
Methods
Internal Review Board approval was obtained for a retro-
spective study of preterm infants who were evaluated and/
or underwent treatment for threshold or prethreshold
retinopathy of prematurity from January 1, 2000, through
December 31, 2005.
Using Current Procedural Terminology (CPT) and Inter-
national Statistical Classification of Diseases and Related
Health Care Problems, 9th Edition (ICD-9) coding, the
patients were selected from the University of Nebraska
Medical Center database.
Data was collected from four hospitals served by the Uni-
versity of Nebraska Retina Service, covering Nebraska's
two largest cities. This encompasses a metropolitan region
of approximately 750,000.
The main outcome measure was retinal detachment (RD).
Data points collected include date of birth; birth weight;
estimated gestational age (EGA) at birth; multiparity;
EGA, zone, stage, and presence or absence of "plus" dis-
ease at the initial and each subsequent examination;
scheduled follow-up examination dates; intervention
date; laser spots placed per eye; follow-up examinations;
RD, including staging; and complications, including late
RD and cataract.
Univariate association with threshold or prethreshold
treatment (Pre-ETROP and Post-ETROP, respectively)
were assessed using t-tests or Wilcoxon tests for the fol-
lowing variables: EGA at birth, weight at birth, interval
between birth and first examination, interval between
birth and surgery, interval between first examination and
surgery, and number of laser spots. Fisher's exact tests or
χ2 tests were used to determine whether treatment was
associated with RD, cataracts, amblyopia, as well as evalu-
ating the extent of zone, stage, and plus disease when the
decision was made to go for surgery.
For patients who developed RD, Fisher's exact tests were
used to determine if threshold versus prethreshold treat-
ment was associated with extent of zone, stage, and plus
disease, as well as when the decision was made to go for
surgery, grade of RD, and multiparity. Wilcoxon tests were
used to determine if provider treatment was associated
with the number of spots placed on laser surgery, age at
birth, weight at birth, and interval between birth and sur-
gery.
For all patients who received laser ablation treatment, as
well as for patients who developed a RD, provider reliabil-
ity was evaluated using Wilcoxon signed rank tests. This
evaluated the difference between days scheduled between
examinations and actual days elapsed between examina-
tions for each interval between adjacent examinations.
In addition, patients were divided into two groups; one
had more than 7 days between the previous examination

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and the examination that determined surgery, and the
other group had 7 days or less between these examina-
tions. Birth weight and EGA were compared between
these two groups using t-test or Wilcoxon test; and extent
of zone, stage, and plus disease were compared between
these two groups, when a decision was made to go for sur-
gery, using Fisher's exact tests or χ2 tests.
Finally, the average follow-up time for Pre-ETROP and
Post-ETROP groups were evaluated using the Wilcoxon
test.
Results
Of the 1045 patients examined during the six year inter-
val, 581 patients were examined prior to adoption of the
ETROP guidelines in December 2003 (group A), with an
additional 464 patients evaluated after adoption of the
ETROP guidelines (Group B). Twenty nine of the 581
(5%) were treated with laser photocoagulation (Pre-
ETROP Group), while 53 of the 464 patients (11.4%)
evaluated after adoption of the ETROP guidelines received
PRP (Post-ETROP Group).
The average EGA at birth of the Pre-ETROP patients was
26.3 weeks, while the average EGA at birth of Post-ETROP
patients was significantly lower at 25.2 weeks (P =
0.0012) (Table 1). Post-ETROP treated infants also had a
significantly lower birth weight, measuring 707 grams ver-
sus 888 grams in the Pre-ETROP group (P = 0.0007)
(Table 1).
The average interval from birth to laser treatment
increased in the Post-ETROP group, from 73 days in the
Pre-ETROP group to 80 days in the Post-ETROP group.
This difference did not reach statistical significance (P =
0.09) (Table 1). However, the interval between the first
screening examination and laser treatment was greater in
the Pre-ETROP group (37 days) than in the Post-ETROP
group (30 days) (P = 0.05) (Table 1).
The amount of plus disease in treated eyes was found to
be significantly higher in the Post-ETROP group (46%) as
compared to the Pre-ETROP group (10%) (P = 0.0001)
(Table 2). There was no statistically significant difference
between Pre-ETROP and Post-ETROP groups in relation
to the follow-up findings of amblyopia or cataract. Multi-
parity was also not found to be a significant variable.
Finally, there was no statistically significant difference in
the number of laser spots placed per eye (Table 1).
The percentage of treated eyes developing Stage 5 RD was
significantly lower in the Post-ETROP group (2 of 106
eyes, 1.9%) as compared to the Pre-ETROP group (6 of 58
eyes, 10.3%) (P = 0.02). The percentage of patients treated
with laser (as opposed to eyes) developing stage 5 RD was
also lower in the Post-ETROP group (2 of 53 patients,
3.8%) than in the Pre-ETROP group (3 of 29
patients,10.3%), though this difference did not reach sta-
tistical significance (P = 0.34) (Figure 1 and Table 2). Cat-
aracts were identified in 6.9% of Pre-ETROP patients (2 of
29), and 3.8% of Post-ETROP patients (2 of 53) (P =
0.61).
When examining serial records during the data collection
phase, it was noted that some infants seemed to progress
rapidly to threshold or pre-threshold disease and were fol-
lowed more closely, while other infants developed clini-
cally significant disease more gradually and were followed
using standard follow-up dates based on the zone, stage,
and plus component of the ROP. To evaluate whether the
greater spacing in days between examinations was due to
different patient characteristics, patients were divided into
two groups; one had greater than 7 days between the pre-
vious examination and the examination that determined
laser surgery, and the other group was 7 days or less
between these examinations. Table 3 demonstrates no sta-
tistically significant difference in either gestational age at
birth or birth weight between those two groups. A non-
significant trend was noted for closer follow up for
Table 1: Characteristics of Pre-ETROP and Post-ETROP Groups
Pre-ETROP Post-ETROP
N = 29
Mean (SD)
26.3 (1.7)
36 (9.54)
888 (257.79)
73 (12.6)
37 (13.72)
1595 (703.2)
1686 (683.63)
5
N = 53
Mean (SD)
25.2 (1.38)
49.5 (18.76)
707 (194.79)
80 (18.34)
30 (18.91)
1698 (499.4)
1573 (491.32)
8
Characteristic
Age at birth, in weeks gestation
Interval between birth and examination 1, in days
Weight at birth, in grams
Interval between birth and laser surgery, in days
Interval between examination 1 and laser surgery, in days
Number of laser spots, right eye
Number of laser spots, left eye
Multiparity
p-value
0.0012
0.0004
0.0007
0.09
0.05
0.46
0.41
0.99
Table 1 demonstrates the characteristics of Pre-ETROP and Post-ETROP Groups treated with laser. Statistically significant differences include age
at birth, weight at birth, and the interval between birth and first examination. Fewer days were needed between the first examination and laser
surgery (P = 0.05). No significant difference was found in the number of laser spots placed, nor in the prevalence of multiparity.

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patients of younger gestational age at birth, and smaller
birth weight.
Analysis of the eyes treated with laser that developed RD
was performed, comparing Pre-ETROP and Post-ETROP
groups with respect to the zone, stage, and the presence of
plus disease at the examination which determined laser
surgery. As demonstrated in Table 4, there was no statisti-
cally significant difference found when comparing RD
eyes by right eye versus left eye, by zone, or by stage. There
was a statistically significant difference in the amount of
plus disease in Post-ETROP versus Pre-ETROP patients
(100% versus 40%, respectively) (P = 0.04). The Pre-
ETROP Group had one twin (3.57%) and the Post-ETROP
Group had four twins (8.16%). There is no statistical evi-
dence of difference in the rate of twins between two
groups (p-value = 0.65).
To evaluate whether poor structural outcome could have
resulted from failure to follow-up with serial examina-
tions, the patients who developed RDs were evaluated
with respect to the number of days scheduled between
examinations versus the actual number of elapsed days
between examinations. This was performed for both Pre-
and Post-ETROP groups combined. Table 5 demonstrates
the data analysis, which fails to find any aberration that
reaches statistical significance.
The average follow up time for Pre-ETROP and Post-
ETROP groups was 492 days and 253 days respectively.
Although there was a tendency for the Pre-ETROP subjects
to be followed for a longer period of time, there was no
statistically significant difference when comparing the two
groups' follow-up time (P = 0.09) (Table 6).
Discussion
Our experience shows that after the ETROP guide-
lineswere implemented, there was a decrease from 11% to
1.9% of eyes developing Stage 5 RD, in spite of this group
having a lower average EGA and lower average birth
weight. The average EGA at birth trended downward, from
26.3 weeks in the Pre-ETROP group, to 25.2 weeks in the
Table 2: Outcomes of Pre-ETROP and Post-ETROP Groups following treatment with laser photocoagulation
Pre-ETROP Post-ETROP
N = 29, eyes = 58
Frequency of RD (%)
5 (17.2)
4 (13.8)
4 (13.8)
3 (10.3)
6 (10.3)
2 (6.9)
2 (6.9)
10 (34.5)
N = 53, eyes = 106
Frequency of RD (%)
8 (15.1)
7 (13.2)
6 (11.3)
2 (3.8)
2 (1.9)
2 (3.8)
0 (0)
46 (86.8)
Outcome
Patients with any RD (retinal detachment)
Right eye
Left eye
Patients with Stage 5 RD
Eyes with Stage 5 RD
Cataracts
Amblyopia
Plus disease before surgery
p-value
0.99
0.99
0.74
0.34
0.02
0.61
0.12
< 0.0001
Evaluation of outcomes of Pre-ETROP and Post-ETROP patients treated with laser photocoagulation. Pre-ETROP and Post-ETROP Groups had 29
and 53 patients and 58 and 106 eyes treated with laser, respectively. A significant decrease was found when analyzing Post-ETROP eyes that
developed Stage 5 RD (P = 0.02). This trend was true for the percentage of Post-ETROP patients as well, though it did not reach statistical
significance. The amount of plus disease in the Post-ETROP group was found to be significantly higher. No difference was found between Pre- and
Post-ETROP Groups with respect to cataracts, amblyopia, multiparity, or when comparing outcomes of right eye versus left eye.
Comparison of Stage 5 RD development between treatment groups
Figure 1
Comparison of Stage 5 RD development between
treatment groups. Percentage of patients (left) and eyes
(right) developing Stage 5 RD. There was a significantly lower
incidence of Stage 5 RD in eyes of Post-ETROP vs. Pre-
ETROP patients (right, P = 0.02). The incidence of Stage 5 RD
was lower in Post-ETROP vs. Pre-ETROP patients (left),
though this difference did not reach statistical significance (P
= 0.34).

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Post-ETROP group (P = 0.0012). This is not an unex-
pected trend, given the increasing survival of preterm
infants under the care of our neonatal colleagues. These
results underscore the importance of adoption of the
ETROP guidelines for treatment.
The percentage of infants having treatment increased from
5% to 11.4%. Despite increased treatment, there was no
appreciable offsetting detrimental effect from treating
twice as many infants. Evaluation of our results showed
no increase in patients developing cataracts under the
ETROP guidelines; in fact, there is a non-statistically sig-
nificant trend toward fewer cataracts in Post-ETROP as
compared to Pre-ETROP patients (3.8% versus 6.9%, P =
0.61). Thus, it is reasonable to assume the benefit of
increased treatment in patients who are treated according
to the recommendations of the ETROP randomized trial
outweighs any unrecognized detrimental effect.
Our data showed a statistically significant difference when
examining the percentage of eyes that developed Stage 5
ROP. These results are consistent with results from the
ETROP trial, which demonstrated a reduction in unfavo-
rable structural outcomes from 15.6% to 9.1% (P < 0.001)
[8].
There was a trend toward a longer interval between birth
and laser treatment in Post-ETROP patients (Table 1),
although it did not reach statistical significance. This most
likely reflects the fact that infants in the Post-ETROP
group had a lower EGA on average than those in the Pre-
ETROP group. In contrast, there was a shorter interval
between the first examination and laser treatment in Post-
ETROP (30 days) versus Pre-ETROP patients (37 days).
This is likely a consequence of the Early Treatment guide-
lines (prethreshold disease appearing earlier than thresh-
old disease).
Table 3: Timing of Examinations with relationship to EGA and birth weight
Greater-than-7-day
group (N = 26)
N
Less-or-equal-7-day
group (N = 56)
N
p-value
Mean (range)SD Mean (range) SD
Age at birth, in weeks
gestation
Weight at birth
2625.92 (24–28) 1.47 5525.44 (23–30) 1.640.14
26782.88 (396–1278)231.22 54767.39 (355–1347) 238.70.73
The examination that determines laser surgery (usually the same day or next day) may be related to age at birth or weight at birth. A trend was
noted toward younger patients of less birth weight being followed more closely, but this did not reach statistical significance.
Table 4: Eye condition on final examination before laser surgery for patients who developed RD.
CharacteristicPre-ETROP (N = 4)
Frequency (%)
Post-ETROP (N = 8)
Frequency (%) p-value
Eye condition before surgery
OD zone
1
2
3
OS zone
1
2
3
OD stage
1
2
3
OS stage
1
2
3
Plus disease
0.99
1 (25)
3 (75)
0 (0)
2 (25)
6 (75)
0 (0)
0.99
1 (25)
3 (75)
0 (0)
2 (25)
6 (75)
0 (0)
0.41
1 (25)
0 (0)
3 (75)
0 (0)
2 (25)
6 (75)
1 (25)
0 (0)
3 (75)
2 (n = 5) (40)
0 (0)
3 (37.5)
5 (62.5)
8 (100) 0.04
Table 4 evaluates the pre-treatment findings in patients who developed a RD. Comparison between Pre- and Post-ETROP Groups demonstrate a
statistically significant increase in the presence of plus disease in Post-ETROP patients as compared to Pre-ETROP patients. No other statistically
significant differences were found.

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In addition, Post-ETROP patients had an increase in the
amount of plus disease, as compared to Pre-ETROP
patients. This may reflect the earlier gestational age at
birth, the smaller birth weight, or simply the increased
emphasis on the presence or absence of plus disease in the
treatment algorithm of the ETROP guidelines protocol.
The emphasis on presence or absence of plus disease in
the ETROP guidelines may also contribute to the noted
increase in plus disease.
Every effort was made to ensure that different providers
did not unduly influence the outcome data. There is no
difference in the number of laser spots placed between
groups or with respect to the treated eye (Table 1). Fur-
ther, there was no statistically significant difference found
between providers in scheduled days versus actual elapsed
days between examinations (Table 5), nor in the differ-
ence in the median follow-up time between the two
groups (Table 6). These criteria are important when com-
paring patients treated by three different surgeons at our
institution in the prethreshold versus threshold treatment
arms.
Strengths of this study include careful evaluation of pro-
vider variability, and analysis of baseline characteristics of
patients who developed poor structural outcome. The pri-
mary weakness of this study is related to the retrospective
analysis. In addition, a larger sample size would further
strengthen data that trended toward, but did not reach,
statistical significance.
Conclusion
In summary, we found a statistically significant difference
in the outcome of ROP eyes treated under the ETROP cri-
teria. Despite possible over-treatment, structural out-
comes have improved, suggesting that the benefit of
treating ROP in high-risk prethreshold disease outweighs
the possible risks of over-treatment in a given high-risk
population. Continuing investigation will allow for deter-
mination of even more specific high-risk factors for devel-
opment of poor structural and visual outcome, narrowing
the targeted high-risk population.
Competing interests
The authors declare that they have no competing interests.
The authors have no proprietary interests in the materials
discussed.
Table 5: Scheduled versus actual days elapsed between examinations for patients treated with laser who developed a retinal
detachment
Number of days
scheduled between
examinations
N
Actual days elapsed
between examinations
p-value
Mean (range) SDN Mean (range)SD
Pre-ETROP Examination numbers
E1–E2
E2–E3
E3–E4
E4–E5
E1–E2
E2–E3
E3–E4
E4–E5
5
5
3
2
7
7
3
2
15.4 (14–21)
10.2 (2–14)
5 (1–7)
0.5 (0–1)
9 (7–14)
5.43 (1–14)
7.33 (1–14)
7 (7-7)
3.13
5.5
3.46
0.71
3.42
4.83
6.51
0
5
3
2
0
7
4
2
2
14.2 (7–22)
16 (6–28)
7.5 (7–8)
--
8.57 (4–14)
7.25 (5–11)
11 (8–14)
7.5 (2–13)
5.31 0.99
0.99
0.99
--
0.72
0.25
0.99
0.99
--
4.08
2.63
4.24
7.78
Post-ETROP
Pre- and Post-ETROP Groups are compared to determine whether there is any discrepancy between the number of days scheduled between
examinations, and the actual number of days elapsed, in patients treated with laser who subsequently developed a RD. Data was analyzed to assess
provider reliability, to determine whether an outlier exists, and if so, could it be a confounding variable in the difference in outcomes between Pre-
and Post-ETROP Groups. No such outlier was found. (E1 = examination # 1, E2 = examination # 2, etc).
Table 6: A Comparison of Folllow-up time between Pre-ETROP and Post-ETROP Groups.
GroupNMean Std Dev Std ErrorMedianMinimum Maximum
Pre-ETROP
Post-ETROP
28
52
491.75
253.37
599.47
266.28
113.29
36.93
304
164
1
14
2450
1135
Wilcoxon Two-Sample Test p-value: 0.09.
A Comparison of Follow-up time between Pre-ETROP and Post-ETROP groups. There is no statistical evidence of difference in the median of
follow-up time between the two groups. While the Post-ETROP group showed shorter follow-up time than the Pre-ETROP Group, this was not
statistically significant at the 0.05 level.

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Authors' contributions
AA participated in patient care, carried out the back-
ground research, generated the database, and drafted the
manuscript and subsequent revisions. MM participated in
the background research, generated the database, and
developed the graphics. TH participated in patient care
and revised the manuscript. JM provided statistical analy-
sis. FQ provided statistical analysis. DI participated in
patient care. EM participated in patient care, drafted the
initial inquiry, participated in background research and
database formation, and guided the revision and submis-
sion process.
Acknowledgements
This research was supported in part by an unrestricted grant from
Research to Prevent Blindness.
Special thanks to Carl Camras, MD, Chairman, Department of Ophthalmol-
ogy and Visual Sciences, University of Nebraska Medical Center, Omaha
Nebraska, USA.
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Pre-publication history
The pre-publication history for this paper can be accessed
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http://www.biomedcentral.com/1471-2415/8/23/prepub