
DOI:10.18240/ijo.2019.07.26
Citation: Villegas
VM, Schwartz SG, Berrocal AM, Murray TG, Flynn HW. Widefield optical
coherence tomography of foveal dragging in retinopathy of prematurity. Int J
Ophthalmol 2019;12(7):1219-1223
·Letter
to the Editor·
Widefield
optical coherence tomography of foveal dragging in retinopathy of prematurity
Victor M. Villegas1, Stephen G. Schwartz1,
Audina M. Berrocal1, Timothy G. Murray2, Harry W. Flynn
Jr.1
1Bascom
Palmer Eye Institute, University of Miami Miller School of Medicine, Miami,
Florida 33136, USA
2Murray
Ocular Oncology and Retina, Miami, Florida 33143, USA
Correspondence
to: Victor M.
Villegas. 900 NW17th Street, Miami, FL 33136, USA. v.villegas@med.miami.edu
Received:
2018-10-23 Accepted:
2018-12-25
DOI:10.18240/ijo.2019.07.26
Citation: Villegas
VM, Schwartz SG, Berrocal AM, Murray TG, Flynn HW. Widefield optical
coherence tomography of foveal dragging in retinopathy of prematurity. Int J
Ophthalmol 2019;12(7):1219-1223
Dear Editor,
Despite
substantial advances in neonatal medicine, retinopathy of prematurity (ROP)
continues to be a serious therapeutic challenge[1].
Visual acuity loss in patients with ROP has been associated with structural
retinal abnormalities (including retinal detachment, retinal folds, and
pigmentary retinopathy), cataract, glaucoma, and amblyopia due to refractive
error or strabismus[2]. A subset of patients with
ROP, either treated or untreated may develop temporal dragging of the fovea.
The reported incidence of foveal dragging varies widely, but can be affected by
retinal photocoagulation and the prematurity level of the infant. For example,
a recent study reported an incidence of 7% in subjects that were treated for
threshold ROP, but
0 in subjects
with spontaneous regression[3]. In the Multicenter
Trial of Cryotherapy for Retinopathy of Prematurity, the most common
association with an unfavorable visual outcome despite a favorable anatomical
outcome was foveal dragging as defined by the Reese cicatricial grading system[4-5]. These subjects have widely
variable visual outcomes. The purpose of the current study is to illustrate
various clinical and imaging findings associated with foveal dragging in
subjects with a history of ROP.
An
Institutional Review Board (IRB)-approved study was performed according to the
Declaration of Helsinki. The Institutional Review Board waived the consenting
process due to retrospective nature and minimal risk. A non-consecutive
non-comparative case series of patients with clinical foveal dragging and
history of ROP examined at a satellite office of a University Referral-Center
was conducted. Data regarding gender, age at examination, medical history,
best-corrected visual acuity (BCVA), fundus photography, and spectral domain
optical coherence tomography (SD-OCT) OCT2 module with a wavelength 870 nm and
scan rate of 85 000 Hz (Heidelberg Engineering, Heidelberg, Germany) were
collected. All patients underwent the institutional standard foveal SD-OCT
protocol using a raster line length of
6.0
mm. In addition, an 8.9-mm raster line length scan was also
performed to evaluate the distance from the foveal center to the optic disc.
The distance from the foveal center to the temporal optic disc and to the optic
disc center were measured in the 8.9-mm raster line using commercially
available software (Heidelberg Engineering, Heidelberg, Germany).
Table 1
summarizes the clinical and SD-OCT findings in the current series. Figures 1-6
show the imaging findings in each case.
Table 1
Clinical characteristics and optic disc to fovea distance as measured by
spectral domain optical coherence tomography in the current series mm
Subject |
Age (y) |
Best-corrected visual acuity (OD) |
Best-corrected visual acuity (OS) |
Follow-up (y) |
Other complications |
Temporal disc edge to fovea distance (OD) |
Temporal disc edge to fovea distance (OS) |
Disc center to fovea distance (OD) |
Disc center to fovea distance (OS) |
1 |
6 |
20/25 |
20/30 |
3 |
Myopia |
4.819 |
4.886 |
5.723 |
5.430 |
2 |
6 |
20/30 |
20/30 |
3 |
Myopia |
5.639 |
5.933 |
6.624 |
6.830 |
3 |
7 |
20/40 |
20/40 |
1 |
Hyperopia, nystagmus |
4.798 |
4.880 |
5.356 |
5.458 |
4 |
9 |
20/25 |
20/30 |
5 |
Myopia |
5.562 |
5.754 |
6.359 |
6.672 |
5 |
21 |
20/40 |
20/25 |
2 |
Myopia, nystagmus, esotropia |
5.647 |
4.725 |
6.643 |
5.519 |
6 |
65 |
20/200 |
20/30 |
2 |
Myopia, amblyopia |
7.531 |
5.986 |
8.186 |
6.824 |
Figure 1
Multimodal imaging of subject
1 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
Figure 2
Multimodal imaging of subject
2 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
Figure 3
Multimodal imaging of subject
3 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
Figure 4
Multimodal imaging of subject
4 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
Figure 5
Multimodal imaging of subject
5 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
Figure 6
Multimodal imaging of subject
6 A: Macular SD-OCT infrared image of the right eye
using raster scan lengths of
6.0 mm;
B: Fundus photography of right eye; C: Fundus photography of left eye; D:
Macular SD-OCT infrared image of the left eye using raster scan lengths of
6.0 mm; E: Macular SD-OCT with infrared image
of the right eye using raster scan length of
8.9 mm; F: Macular SD-OCT with infrared image of the
left eye using raster scan length of
8.9 mm.
The majority
of previous studies using SD-OCT to evaluate ROP subjects have focused on
macular features such as retention of the inner retinal layers at the foveal
center, presence of outer nuclear layer widening, photoreceptor elongation,
macular cystoid changes, and abnormalities in foveal development[6-15]. Recent studies have also
described macular schisis, inner retinal thickening, chorioretinal atrophy in
subjects with a history of ROP[16]. However, the
literature regarding the SD-OCT features present in subjects with a history of
ROP and foveal dragging is limited. In the present series, 10/12 eyes had
retention of the inner nuclear layers at the foveal center. All eyes had
presence of outer nuclear layer widening with photoreceptor elongation.
The
literature regarding the distance between the fovea and the optic disc in
normal children and adults is scarce. Prior studies have had differences in
measurement points; some studies measured the disc center-to-fovea distance and
others have measured temporal disc edge-to-fovea distance[17-19]. This discrepancy in measurements could affect the
results by about half a disc diameter (
0.8 mm). A study of 3468 adults in China reported a
mean disc center-to-fovea distance of 4.76±
0.34 mm; this distance increased with increasing axial
length, larger parapapillary alpha zone and parapapillary beta/gamma zone, and
larger disc area[17]. A study performed in
Finland in prematurely born children (aged 10-11y) reported the mean disc
center-to-fovea distance to be 4.74±
0.29 mm[18]. Another
study performed in England that analyzed preterm and full-term infants reported
a mean temporal disc edge-to-fovea distance of 4.4±
0.4 mm, without difference between the preterm infants
and the full-term infants[19]. This slightly
lower mean in infants may be associated with shorter axial length. Based on the
historical data, an SD-OCT infrared image with a raster line length of
6.0 mm should visualize the optic nerve in
most normal subjects.
In the
present series, all eyes were two standard deviations above historical controls
when disc center-to-fovea distance and temporal disc edge-to-fovea distance
were compared[17-19]. In 5/6
subjects, the ROP was treated with photocoagulation and in one ROP regressed
spontaneously. The SD-OCT infrared image failed to visualize the optic nerve
head in 11/12 eyes due to temporal foveal dragging; the exception was Subject 5
OS, in which only the temporal edge of the disc is visible. Failure to visualize
the optic nerve head in the fundus map photo in the SD-OCT study may represent
a quick test to identify foveal dragging.
The
literature suggests a mean distance from the temporal disc margin to the fovea
of approximately
4.4 mm in
infants and approximately
4.75 mm
in adults; for children aged 6-7y, perhaps an intermediate value would be
appropriate. In the present series, 4 patients were aged 6-9y; of these, 2 had
distances of about
4.8 mm in
each eye and 2 had a distance greater than
5.6 mm in each eye. Also in the present series, there
were 2 adult patients; in 1, distances were
4.7 mm in 1 eye and
5.6 mm in the other; in the other adult, distances
were greater than
5.6 mm in
each eye. In summary, all eyes in this series had disc-to-fovea distances
greater than historical controls.
The
cicatricial stage of ROP retinopathy can lead to lenticular myopia, temporal
vitreoretinal fibrosis, dragging of the macula, and vitreoretinal folds.
Therefore, cicatricial ROP may alter the normal fundus landmarks and may affect
the results of the measurements carried out on fundus photographs[20]. Previous studies that have evaluated the
disc-to-fovea distance have used fundus photography to estimate the distance[17-19]. However, the present study
used SD-OCT to measure the distance using a raster line length of
8.9 mm. SD-OCT may allow for improved
accuracy in measurements, especially in eyes with a posterior pole staphyloma.
In the
current study, the standard foveal SD-OCT protocol uses a raster line length of
6.0 mm. Normally the optic
nerve is visible in the infrared image centered on the fovea. The optic nerve
was not completely visible in the infrared fundus image in any of the eyes
reported in this study (Figures
1A,
1D,
2A, 2D,
3A, 3D,
4A, 4D,
5A,
5D,
6A, 6D). In one eye of subject
5, the fundus infrared image showed the temporal optic nerve head (Figure 5D).
The present
study is limited by the retrospective and nonconsecutive nature of the case
series, as well as selection bias because only patients that could cooperate
for SD-OCT scans were included. Most patients in our series had mild clinical
features of foveal dragging and it is likely that some patients with advanced
foveal dragging and poor visual acuity could not undergo SD-OCT scanning, due
to poor fixation or poor cooperation, and may have been missed by the study
design. In addition, there is no specific ICD-10 code for foveal dragging, so
it is very likely that other patients with this entity were not captured. This
series is not comprehensive, but it does illustrate many pertinent features of
this diagnosis. Larger series with age-matched controls may help identify the
spectrum of foveal dragging distance that may be associated with variable
clinical and visual outcomes.
In
conclusion, some subjects with history of ROP may have an increased
disc-to-fovea distance. SD-OCT can aid in the detection of this anomaly, and
the distance may be measured using commercially available software. Further
studies with longer follow up and larger cohorts may lead to a better
understanding of this condition.
ACKNOWLEDGEMENTS
This
manuscript was presented as a poster at the AAO 2017.
Foundations: Supported in part by the National
Institute of Health, Bethesda, Maryland (Grant P30-EY014801); an unrestricted
grant to the University of Miami from Research to Prevent Blindness, New York,
New York, USA.
Conflicts of
Interest: Villegas VM, None; Schwartz SG, Consultant: Alimera, Bausch and
Lomb, Welch Allyn; Berrocal AM, Consultant: Dutch Ophthalmic Research
Center, Visunex, Alcon; Murray TG, None; Flynn HW, None.
REFERENCES
1 Gilbert C. Changing challenges
in the control of blindness in children. Eye (Lond) 2007;21(10):1338-1343.
https://doi.org/10.1038/sj.eye.6702841
PMid:17914437 |
|
2 Shah PK, Prabhu V, Karandikar
SS, Ranjan R, Narendran V, Kalpana N. Retinopathy of prematurity: Past,
present and future. World J Clin Pediatr 2016;5(1):35-46.
https://doi.org/10.5409/wjcp.v5.i1.35
PMid:26862500 PMCid:PMC4737691 |
|
|
3 Sahni J, Subhedar NV, Clark D.
Treated threshold stage 3 versus spontaneously regressed subthreshold stage 3
retinopathy of prematurity: a study of motility, refractive, and anatomical
outcomes at 6mo and 36mo. Br J Ophthalmol 2005;89(2):154-159.
https://doi.org/10.1136/bjo.2004.045815
PMid:15665344 PMCid:PMC1772499 |
|
|
4 Gilbert WS, Dobson V, Quinn GE,
Reynolds J, Tung B, Flynn JT. The correlation of visual function with
posterior retinal structure in severe retinopathy of prematurity. Cryotherapy
for Retinopathy of Prematurity Cooperative Group. Arch Ophthalmol
1992;110(5):625-631.
https://doi.org/10.1001/archopht.1992.01080170047022
PMid:1580837 |
|
|
5 Classification of retrolental
fibroplasia. Am J Ophthalmol 1953;36(10): 1333-1335.
https://doi.org/10.1016/0002-9394(53)90791-0 |
|
|
6 Villegas VM, Capó H, Cavuoto K,
McKeown CA, Berrocal AM. Foveal Structure-Function correlation in children
with history of retinopathy of prematurity. Am J Ophthalmol 2014;158(3):508-512.e2.
https://doi.org/10.1016/j.ajo.2014.05.017
PMid:24874998 |
|
|
7 Dubis AM, Subramaniam CD, Godara
P, Carroll J, Costakos DM. Subclinical macular findings in infants screened
for retinopathy of prematurity with spectral-domain optical coherence
tomography. Ophthalmology 2013;120(8):1665-1671.
https://doi.org/10.1016/j.ophtha.2013.01.028
PMid:23672969 PMCid:PMC3737379 |
|
|
8 Maldonado RS, O'Connell R,
Ascher SB, Sarin N, Freedman SF, Wallace DK, Chiu SJ, Farsiu S, Cotten M,
Toth CA. Spectral-domain optical coherence tomographic assessment of severity
of cystoid macular edema in retinopathy of prematurity. Arch Ophthalmol
2012;130(5):569-578.
https://doi.org/10.1001/archopthalmol.2011.1846
PMid:22232366 PMCid:PMC3515869 |
|
|
9 Erol MK, Ozdemir O, Turgut Coban
D, Bilgin AB, Dogan B, Sogutlu Sari E, Toslak D. Macular findings obtained by
spectral domain optical coherence tomography in retinopathy of prematurity. J
Ophthalmol 2014;2014:468653.
https://doi.org/10.1155/2014/468653
PMid:25544895 PMCid:PMC4269090 |
|
|
10 Joshi MM, Trese MT, Capone A
Jr. Optical coherence tomography findings in stage 4A retinopathy of
prematurity: a theory for visual variability. Ophthalmology
2006;113(4):657-660.
https://doi.org/10.1016/j.ophtha.2006.01.007
PMid:16581425 |
|
|
11 Gursoy H, Bilgec MD, Erol N,
Basmak H, Colak E. The macular findings on spectral-domain optical coherence
tomography in premature infants with or without retinopathy of prematurity.
Int Ophthalmol 2016;36(4):591-600.
https://doi.org/10.1007/s10792-016-0176-9
PMid:26750097 |
|
|
12 Hammer DX, Iftimia NV, Ferguson
RD, Bigelow CE, Ustun TE, Barnaby AM, Fulton AB. Foveal fine structure in
retinopathy of prematurity: an adaptive optics Fourier domain optical
coherence tomography study. Invest Ophthalmol Vis Sci 2008;49(5):2061-2070.
https://doi.org/10.1167/iovs.07-1228
PMid:18223243 PMCid:PMC2923467 |
|
|
13 Wu WC, Lin RI, Shih CP, Wang
NK, Chen YP, Chao AN, Chen KJ, Chen TL, Hwang YS, Lai CC, Huang CY, Tsai S.
Visual acuity, optical components, and macular abnormalities in patients with
a history of retinopathy of prematurity. Ophthalmology 2012;119(9):1907-1916.
https://doi.org/10.1016/j.ophtha.2012.02.040
PMid:22578258 |
|
|
14 Vinekar A, Avadhani K,
Sivakumar M, Mahendradas P, Kurian M, Braganza S, Shetty R, Shetty BK.
Understanding clinically undetected macular changes in early retinopathy of
prematurity on spectral domain optical coherence tomography. Invest
Ophthalmol Vis Sci 2011;52(8):5183-5188.
https://doi.org/10.1167/iovs.10-7155
PMid:21551410 |
|
|
15 Muni RH, Kohly RP, Charonis AC,
Lee TC. Retinoschisis detected with handheld spectral-domain optical
coherence tomography in neonates with advanced retinopathy of prematurity.
Arch Ophthalmol 2010;128(1):57-62.
https://doi.org/10.1001/archophthalmol.2009.361
PMid:20065217 |
|
|
16 Thanos A, Yonekawa Y, Todorich
B, Huang N, Drenser KA, Williams GA, Trese MT, Capone A Jr. Spectral-domain
optical coherence tomography in older patients with history of retinopathy of
prematurity. Ophthalmic Surg Lasers Imaging Retina 2016;47(12):1086-1094.
https://doi.org/10.3928/23258160-20161130-02
PMid:27977831 |
|
|
17 Jonas RA, Wang YX, Yang H, Li
JJ, Xu L, Panda-Jonas S, Jonas JB. Optic disc-fovea distance, axial length
and parapapillary zones. The Beijing Eye Study 2011. PLoS One
2015;10(9):e0138701.
https://doi.org/10.1371/journal.pone.0138701
PMid:26390438 PMCid:PMC4577126 |
|
|
18 Knaapi L, Lehtonen T, Vesti E,
Leinonen MT. Determining the size of retinal features in prematurely Born
children by fundus photography. Acta Ophthalmol 2015;93(4):339-341.
https://doi.org/10.1111/aos.12554
PMid:25270671 |
|
|
19 De Silva DJ, Cocker KD, Lau G,
Clay ST, Fielder AR, Moseley MJ. Optic disk size and optic disk-to-fovea
distance in preterm and full-term infants. Invest Ophthalmol Vis Sci
2006;47(11):4683-4686.
https://doi.org/10.1167/iovs.06-0152
PMid:17065474 |
|
|
20 Rohrschneider K. Determination
of the location of the fovea on the fundus. Invest Ophthalmol Vis Sci
2004;45(9):3257-3258.
https://doi.org/10.1167/iovs.03-1157
PMid:15326148 |
|