Retinal and Choroidal Thickness in Children with a History of Retinopathy of Prematurity and Transscleral Diode Laser Treatment

Abstract

Purpose

To evaluate the outcomes of transscleral diode laser photocoagulation in the eyes of children with a history of threshold retinopathy of prematurity (ROP) and compare them with the eyes of children with no or subthreshold ROP and normal term infants by spectral-domain optical coherence tomography (SD-OCT).

Methods

Three groups of children aged 4 to 10 years were included as follows: 45 patients with regressed ROP who had not received any treatment (group 1), 48 patients with a history of zone 2 threshold ROP who had been treated with transscleral diode laser (group 2), and 56 age-matched healthy full-term children (group 3). Visual acuity, refractive error, and measurement of retinal and choroidal thickness by SD-OCT were compared between groups retrospectively.

Results

The mean gestational age (GA) and birthweight (BW) were 31 weeks and 1,409 grams in group 1, 28.7 weeks and 1,274.5 grams in group 2, and 38.4 weeks and 3,285 grams in group 3, respectively. There were 6 significant differences in the laser group: GA, BW, macular thickness, foveal depression, spherical equivalent, and visual acuity. In contrast, there were no significant differences among any of the choroidal parameters in all of the groups. Neither macular nor choroidal thickness correlated with visual acuity.

Conclusions

Although retinal structural changes were observed in patients with a history of ROP, especially in patients treated with laser, no significant difference was found in choroidal thickness between groups. These structural abnormalities may be related to both severity of ROP and laser treatment.

Keywords

Choroidal thickness Retinal thickness Retinopathy of prematurity Spectral-domain optical coherence tomography Transscleral diode laser photocoagulation

Introduction

Retinopathy of prematurity (ROP) is a vasoproliferative disease of the retina among preterm infants. The increasing immaturity of these infants has left them at a much higher risk of developing ROP (1, 2). Although most cases regress spontaneously, some advanced cases progress to retinal detachment. The main purpose of treatment is to prevent neovascularization and complications secondary to neovascularization and 2 large randomized clinical trials have demonstrated that ablation of the avascular retina is an effective treatment to prevent progression of ROP (3, 4).

The ablation of the peripheral retina by transpupillary diode laser is the current standard care for the treatment of threshold ROP and transscleral cryotherapy has been replaced by transpupillary and transscleral diode laser photocoagulation. As transscleral cryotherapy is associated with complications such as ocular inflammation, choroidal damage, and breakdown of the blood-retinal barrier and transpupillary diode laser is associated with complications such as lenticular opacities and cataract formation, transscleral diode laser photocoagulation has been used as an alternative treatment method of ablation with satisfactory results (5–6–7–8).

Either the presence of ROP or prematurity without a history of ROP can cause visual deficits, even in the absence of pathology on ophthalmoscopy (9, 10). Studies using optical coherence tomography (OCT) have revealed the effect of both prematurity and ROP on macular anatomy and have shown retention of the inner retinal layers at the foveal center, absence of foveal depression, and thickening of the central macula in preterm infants; however, association between these reported structural changes and poorer visual acuity in prematurely born children remains unclear (11–12–13). It has been suggested that nonretinal visual system abnormalities or changes other than macular changes could cause visual disruption in prematurely born children (9, 11).

The choroid contributes oxygen and nutrients to the outer retina and the involvement of the choroid in ROP would explain the associated functional deficit (14). The development of enhanced depth imaging (EDI) with spectral domain (SD) OCT has improved the visualization of the choroid, and has demonstrated a thinner choroid in prematurely born children, in contrast to increased foveal thickness. An association between decreased choroidal thickness and worse vision in patients with a history of ROP also remains unclear (11, 15, 16).

In this study, macular and choroidal thickness profiles were evaluated using SD-OCT with an EDI technique. We compared patients born prematurely who had a history of regressed ROP and patients with a history of zone 2 threshold ROP who had received transscleral diode laser treatment with full-term healthy children.

Methods

The study involved 3 groups of children aged 4 to 10 years: preterm children with regressed ROP, preterm children with a history of zone 2 threshold ROP, and age-matched healthy, full-term children, who were examined at the Istanbul Retina Institute between January 1, 2014, and June 30, 2015. The preterm children with regressed ROP were included if they had a gestational age 37 weeks or less and if their follow-up had continued until ROP had resolved completely without any treatment. Inclusion criteria for preterm children with zone 2 threshold ROP was transscleral diode laser treatment in infancy with follow-up since then at the Istanbul Retina Institute. The full-term children were included if they had a gestational age more than 37 weeks and birthweight over 2,500 g. The fundi of all eyes were normal in appearance except preterm children with a history of zone 2 threshold ROP who had laser burns at peripheral retina. Patients with a history of eye trauma or surgery, cerebral damage, congenital defects, or ocular disease such as amblyopia, strabismus, nystagmus, cataract, glaucoma, or retinal detachment were excluded from the study. Both eyes of each participant were examined, but data from only one eye, which was selected randomly, were included in the study. The research followed the tenets of the Declaration of Helsinki. Informed consent was obtained from the subjects after explanation of the nature and possible consequences of the study. The research was approved by the institutional review board.

Optical coherence tomography images were obtained by a single, masked examiner experienced in performing scans using the SD-OCT device (Heidelberg Engineering, Heidelberg, Germany). To exclude diurnal variations, all examinations were performed at the same time of day (11 AM-1 PM). High-quality horizontal and vertical line scans centered on the fovea were obtained for each eye, with 100 frames averaged using automatic averaging. The foveal thickness was defined as the distance between the internal limiting membrane and the inner border of the retinal pigment epithelium. The central foveal thickness and the thickness 1.0 mm, 2.0 mm, and 3.0 mm from the fovea, in the nasal, temporal superior, and inferior regions, were measured. The average of 14 thickness recordings was accepted as the macular retinal thickness. The foveal depression was determined by subtracting the central foveal thickness from the mean parafoveal thickness. Values less than 56.4 µm were identified as an absence of foveal depression (12). The choroidal thickness was defined as the distance between the base of the retinal pigment epithelium and the choroidoscleral boundary. Each measurement was performed at the fovea and 1.0, 2.0, and 3.0 mm nasal, temporal, superior, and inferior to the fovea using the manual calipers provided with the software of the device. The average of 14 choroidal thickness recordings was accepted as the macular choroidal thickness. Ocular axial length was measured using partial coherence laser interferometry (IOLMaster, Carl Zeiss Meditec, La Jolla, CA, USA). Each choroidal thickness from the horizontal and vertical line scans was measured by 2 of the coauthors, and values were averaged.

The data from patient medical records, including relevant demographic and birth data, measurement of best-corrected visual acuity (BCVA) with the Early Treatment Diabetic Retinopathy Study chart, cycloplegic refraction error, detailed anterior segment, and fundus examination by using slit-lamp biomicroscopy with 90-D noncontact lens, macular and choroidal thicknesses, and axial length measurements were collected retrospectively. Data for all patients were used for statistical analysis. Descriptive statistical methods (mean, SD) were used for all characteristics. Chi-square, one-way analysis of variance (ANOVA), and post hoc Tukey tests were used to compare all variables among the 3 groups. Bivariate correlations were evaluated using the Pearson correlation test. p<0.05 Was considered statistically significant.

Results

A total of 149 participants were eligible for inclusion: 45 in the nontreated group (group 1), 48 in the treated group (group 2), and 56 in the control group (group 3) (Tab. I). The mean gestational age and birthweight in the treated group were significantly less than the nontreated group. The birthweight in group 3 was significantly greater than those of the other groups. There was no significant difference in the mean age at the time of examination or the sex distribution among the groups. The mean logMAR BCVA in group 2 was significantly worse than those of the other groups and the mean spherical equivalent was significantly greater. However, there was no significant difference in the axial length between the groups. A foveal depression was absent in 16% of group 1 and 63% of group 2 eyes. There was no significant correlation between logMAR BVCA and other variables, such as gestational age, birthweight, spherical equivalent, and axial length in groups 2 and 3, but there was a significant correlation between logMAR BCVA and birthweight in group 1 (p = 0.008).

TABLE I

Demographic and clinical data from all 3 groups

	Group 1 (n = 45), mean ± SD or n (%)	Group 2 (n = 48), mean ± SD or n (%)	Group 3 (n = 56), mean ± SD or n (%)	p
GA^a, wk	30.96 ± 2.8	28.67 ± 2.6	38.39 ± 0.6	<0.001^b
BW^c, g	1,408.8 ± 525	1,274.5 ± 352.7	3,285.2 ± 431.6	<0.001^b
Age, y	8.1 ± 2.6	8.7 ± 1.7	8 ± 1.8	0.24
Sex
Male	24 (53.3)	24 (50)	32 (57.1)	0.77
Female	21 (46.7)	24 (50)	24 (42.9)
BCVA^d, logMAR	0.1 ± 0.1	0.2 ± 0.1	0.03 ± 0.04	<0.001^b
SE^e, D	0.4 ± 2.1	1.9 ± 2.5	0.3 ± 0.9	<0.001^b
Axial length, mm	22.51 ± 0.9	22.51 ± 1.5	22.74 ± 0.7	0.46
Foveal depression, µm
<56.4	7 (15.6)	30 (62.5)	0 (0)	<0.001^b
≥56.4	38 (84.4)	18 (37.5)	56 (100)
Retinal thickness^f,^g	304.8 ± 12.2	315.9 ± 19.5	302.9 ± 16	<0.001^b
Choroidal thickness^h	306.4 ± 73	294.3 ± 70.6	301.7 ± 60.8	0.684

Group 1 vs group 2 p<0.001; group 1 vs group 3 p<0.001; group 2 vs group 3 p<0.001, post hoc Tukey test.

Significant.

Group 1 vs group 2 p = 0.307; group 1 vs group 3 p<0.001; group 2 vs group 3 p<0.001, post hoc Tukey test.

Group 1 vs group 2 p<0.001; group 1 vs group 3 p<0.001; group 2 vs group 3 p<0.001, post hoc Tukey test.

Group 1 vs group 2 p<0.001; group 1 vs group 3 p = 0.964; group 2 vs group 3 p<0.001, post hoc Tukey test.

Mean macular retinal thickness.

Group 1 vs group 2 p<0.001; group 1 vs group 3 p = 0.842; group 2 vs group 3 p<0.001, post hoc Tukey test.

Mean macular choroidal thickness.

BCVA = best-corrected visual acuity; BW = birthweight; D = diopter; GA = gestational age; SD = standard deviation; SE = spherical equivalent.

The mean foveal and macular thickness and the thickness 2.0 mm and 3.0 mm temporal to the fovea were greatest for group 2 patients (Tab. II). The gestational age (r = -0.33, p = 0.03 and r = -0.50, p<0.001) and birthweight (r = -0.41, p = 0.005 and r = -0.44, p = 0.002) of groups 1 and 2 were inversely correlated with the mean foveal thickness, but not with the mean macular thickness. Analysis of covariance (one-way ANOVA, Bonferroni test with gestational age and birthweight as covariates) was performed and a statistically significant difference was found between groups 1 and 2 (p = 0.002). There was no correlation between the mean macular thickness and logMAR BCVA in either group.

TABLE II

Mean retinal thickness: foveal and macular, µm

Location	Group 1 (n = 45), mean ± SD	Group 2 (n = 48), mean ± SD	Group 3 (n = 56), mean ± SD	p
Horizontal foveal center^a	249.6 ± 36.5	283.3 ± 32.6	216.7 ± 15.1	<0.001^b
Inner nasal^c	348.7 ± 16.1	352.8 ± 34.7	348 ± 11.4	0.525
Middle nasal^d	329.8 ± 15.4	339.8 ± 27.7	330.9 ± 16	0.52
Outer nasal^e	304.7 ± 17	307.7 ± 25.1	308.4 ± 16.9	0.641
Inner temporal^f	334.2 ± 14.1	343.2 ± 28.6	340.8 ± 17.5	0.102
Middle temporal^g,^h	297.6 ± 11.4	316 ± 27.4	302.9 ± 17	<0.001^b
Outer temporalⁱ,^j	260.6 ± 12.4	279.4 ± 24.4	272.7 ± 25.7	<0.001^b
Vertical foveal center^k	250.6 ± 36.2	289.3 ± 33.4	218.6 ± 17.1	<0.001^b
Inner superiorⁱ	357.7 ± 20.4	355 ± 21.3	356.3 ± 26.5	0.857
Middle superior^m	315.1 ± 15.4	323.7 ± 19.5	319 ± 22.4	0.109
Outer superiorⁿ	284 ± 17.4	290.5 ± 19.3	290.9 ± 23.1	0.181
Inner inferior^o	354.1 ± 24.4	353.8 ± 19.2	359.9 ± 18.1	0.227
Middle inferior^p	305.9 ± 27.1	312.5 ± 21	310.1 ± 23.6	0.407
Outer inferior^q	274.4 ± 21.1	275.2 ± 18.8	266 ± 24.2	0.57

Group 1 vs group 2 p<0.001; group 1 vs group 3 p<0.001; group 2 vs group 3 p<0.001, post hoc Tukey test.

Significant.

1.0 mm nasal to the fovea.

2.0 mm nasal to the fovea.

3.0 mm nasal to the fovea.

1.0 mm temporal to the fovea.

Group 1 vs group 2 p<0.001; group 1 vs group 3 p = 0.362; group 2 vs group 3 p = 0.003, post hoc Tukey test.

2.0 mm temporal to the fovea

Group 1 vs group 2 p<0.001; group 1 vs group 3 p = 0.018; group 2 vs group 3 p = 0.275, post hoc Tukey test.

3.0 mm temporal to the fovea.

Group 1 vs group 2 p<0.001; group 1 vs group 3 p<0.001; group 2 vs group 3 p<0.001, post hoc Tukey test.

1.0 mm superior to the fovea.

2.0 mm superior to the fovea.

3.0 mm superior to the fovea.

1.0 mm inferior to the fovea.

2.0 mm inferior to the fovea

3.0 mm inferior to the fovea.

The mean foveal and macular choroidal thickness was less in the treated group than the other groups, but there was no significant difference between groups (Tab. III). The choroidal thicknesses 2.0 mm and 3.0 mm nasal to the fovea were greatest for group 2, but there was no significant difference between groups. The spherical equivalent and axial length were correlated with both the mean foveal (r = 0.45, p = 0.002 and r = 0.54, p<0.001; r = -0.39, p = 0.009 and r = -0.62, p<0.001) and macular choroidal (r = 0.41, p = 0.005 and r = 0.54, p<0.001; r = -0.33, p = 0.03 and r = -0.57, p<0.001) thickness in groups 1 and 2. There was no correlation between the mean choroidal thickness and logMAR BCVA in either group.

TABLE III

Mean choroidal thickness: foveal and macular, µm

Location	Group 1 (n = 45), mean ± SD	Group 2 (n = 48), mean ± SD	Group 3 (n = 56), mean ± SD	p
Horizontal foveal center	311.1 ± 81.2	290.4 ± 81	305.6 ± 68.9	0.391
Inner nasal^a	289 ± 88	281.7 ± 80.1	282.5 ± 71.3	0.888
Middle nasal^b	231.8 ± 77.3	251.6 ± 77.1	235.8 ± 76.1	0.414
Outer nasal^c	162.8 ± 57.7	200 ± 66.9	172.5 ± 56.3	0.052
Inner temporal^d	322.3 ± 76.1	298.9 ± 80.1	312.2 ± 68.5	0.318
Middle temporal^e	323.9 ± 65.6	294 ± 73.7	314.4 ± 70.9	0.113
Outer temporal^f	315.4 ± 56.3	288.1 ± 76.5	312.6 ± 71.7	0.099
Vertical foveal center	336.6 ± 89.6	309.4 ± 88.8	323.6 ± 67.1	0.276
Inner superior^g	340.8 ± 92.6	313.5 ± 84.9	327.8 ± 66.8	0.271
Middle superior^h	343.3 ± 87.3	322.6 ± 85.9	336.4 ± 70.4	0.453
Outer superiorⁱ	340.7 ± 84.9	334.6 ± 82	337.6 ± 68.8	0.932
Inner inferior^j	332.2 ± 101.2	310.8 ± 93.2	323.5 ± 71.1	0.502
Middle inferior^k	325.7 ± 91.9	309.3 ± 83.8	322 ± 69.4	0.591
Outer inferior^l	313.8 ± 79.8	304.6 ± 70.2	317.8 ± 74.7	0.665

1.0 mm nasal to the fovea.

2.0 mm nasal to the fovea.

3.0 mm nasal to the fovea.

1.0 mm temporal to the fovea.

2.0 mm temporal to the fovea.

3.0 mm temporal to the fovea.

1.0 mm superior to the fovea.

2.0 mm superior to the fovea.

3.0 mm superior to the fovea.

1.0 mm inferior to the fovea.

2.0 mm inferior to the fovea.

3.0 mm inferior to the fovea.

The representative OCT images of every group demonstrated differences in foveal depression and method of choroidal thickness measurement (Fig. 1, A–B–C). Scatterplots with regression lines of choroidal thickness vs spherical equivalent and axial length also demonstrated the correlation between those variables (Figs. 2 and 3).

Fig. 1

(A) Horizontal optical coherence tomography scan image shows the method of choroidal thickness measurement at the fovea and 1.0, 2.0, and 3.0 mm nasal and temporal to the fovea and representative image of preterm children with regressed retinopathy of prematurity (ROP) who had not received any treatment. (B) Vertical optical coherence tomography scan image shows the method of choroidal thickness measurement at the fovea and 1.0, 2.0, and 3.0 mm superior and inferior to the fovea and representative image of preterm children with threshold ROP who had been treated with transscleral diode laser. (C) Horizontal optical coherence tomography scan image shows the method of choroidal thickness measurement at the fovea and 1.0, 2.0, and 3.0 mm nasal and temporal to the fovea and representative image of full-term children.

Fig. 2

Scatterplot with regression lines of choroidal thickness vs spherical equivalent demonstrates the correlation between those variables.

Fig. 3

Scatterplot with regression lines of choroidal thickness vs axial length demonstrates the correlation between those variables.

Discussion

It was reported that patients with threshold ROP who had been treated with peripheral ablative procedures had a significantly increased macular thickness, higher incidence of absence of foveal depression, higher refractive errors, and poorer BCVA; however, they had normal axial length (12, 13). It was found that high refractive errors and poorer BCVA were not because of a difference in axial length; rather, they were related to optical component in the anterior segment in treated cases (12). Wu et al (16) and Akerblom et al (17) reported correlation of macular thickness with gestational age at birth, but no significant correlation between macular thickness and sex, age at examination, refractive error, visual acuity, or axial length. Villegas et al (13) found no direct correlation between retinal thickness and gestational age and reported a significant correlation between BCVA and refractive error. In our study, as in previous studies, greater macular thickness, a higher incidence of absence of foveal depression, higher refractive errors, and poorer BCVA were found in patients with treated with transscleral diode laser photocoagulation than those in the other groups. The axial length was also normal but we could not evaluate the optical component in the anterior segment. Other than that, no statistically significant difference for choroidal thickness among groups was found in the present study. Similar to Wu et al (16) and Akerblom et al (17), we found a negative correlation between retinal thickness and gestational age. Besides this, a significant correlation between retinal thickness and birthweight was demonstrated in this study.

It has been suggested that macular morphologic abnormalities such as arrest in foveal development and increased macular thickness are related to prematurity (12, 13, 18, 19). In addition to this, it was speculated that laser treatment to destroy an avascular retina contributed to retinal structural changes, such as increased retinal thickness (12). Similar to the present study, the highest incidence of the absence of foveal depression and greatest mean foveal thickness were reported in patients with a history of ROP who had been treated with ablation (12). The middle and outer temporal thickness were greatest in the treated group as well as macular retinal, horizontal and vertical foveal thickness in the present study. It should be considered because of importance of the temporal locations leading to fovea and macula. These structural changes may be related to both stages of ROP and laser treatment.

Despite an absence of foveal depression, preserved acuity was also reported in patients with a history of ROP (13). Villegas et al (13) reported 20/40 or better BCVA in 64% of eyes, despite an abnormal foveal depression in 91%. In the present study, 91% of premature patients (both group 1 and 2) had 20/40 or better BCVA and 40% had an abnormal foveal depression. This difference between studies may be related to the mean gestational age, which was reported as 25.1 ± 2.2 weeks in the study by Villegas et al (13) and 29.8 ± 2.9 weeks in the present study.

Wu et al (16) reported that patients with ROP requiring treatment had a significantly thinner choroid than patients with ROP with spontaneous regression, and the choroid in the superior and inferior quadrants especially was thinner in patients with a history of threshold ROP. A thinner choroid was also associated with worse vision in patients with ROP (13). However, the mean subfoveal thickness was less in patients with ROP than healthy controls, and no correlation between choroidal thickness and visual acuity was reported in the study by Anderson et al (15). Park and Oh (11) also found a decreased choroidal thickness 3 mm temporal to the fovea in preterm children but no association between those structural changes and visual functions. In addition, correlations between choroidal thickness and spherical equivalent, axial length, and ROP stage were demonstrated. However, there was no correlation between subfoveal choroidal thickness and gestational age and birthweight (11, 15, 16). It was also speculated that the choroidal thinning might be a sequel of the treatment for ROP rather than the condition itself, but no correlation was reported between choroidal thickness and laser treatment in the study by Park and Oh (11). In the present study, no significant difference for choroidal thickness was found among groups, which may support that laser treatment had no effect on choroidal thickness and transscleral diode laser was a safe treatment modality in patients with threshold ROP. There was also no correlation between choroidal thickness and other variables such as gestational age, birthweight, or BCVA, except for spherical equivalent and axial length, which is similar to previous studies.

In conclusion, patients with ROP requiring treatment often have retinal but no choroidal morphologic changes shown on SD-OCT. However, neither macular nor choroidal thickness correlated with visual acuity. These structural abnormalities may be related to both prematurity and laser treatment and have a minor impact on functional results.

Footnotes

Acknowledgment

The authors thank Omer Uysal, PhD, for statistical analysis.

Financial support: No financial support was received for this submission.

Conflict of interest: None of the authors has conflict of interest with this submission.

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