Choroidal thickness and vascularity index in Chinese children with high hypermetropia using optical coherence tomography (OCT)

doi:10.21203/rs.3.rs-1546729/v1

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Choroidal thickness and vascularity index in Chinese children with high hypermetropia using optical coherence tomography (OCT)

https://doi.org/10.21203/rs.3.rs-1546729/v1

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Objectives: The current study was to evaluate the choroidal thickness and vascularity index in Chinese children with high hypermetropia through enhanced depth imaging optical coherence tomography (EDI-OCT).

Methods: Cross-sectional study. A total of 21 children with high hypermetropia and 29 children with normal refractive status were retrospectively enrolled in the study. The measurement of the macular choroidal thickness（CT）, 7 points: the sub-foveal area point, the temporal and nasal points at a radius of 0.5-mm, 1.5-mm, and 3-mm were measured. After binarization of the OCT images, the total choroidal area (TCA), stromal area (SA) as well as the luminal area (LA) were identified and measured. The Choroidal vascularity index (CVI)was defined as the ratio of LA to TCA. The independent t-test for normal distributions and Kruskal-Wallis tests for non-normal distributions were used to compare other parameters between groups. The Tamhane's T2 test was performed to adjust for multiple comparisons between groups within each analysis.

Results: The SFCT in the high hypermetropic group was significantly thicker than that in normal controls (371.32 ± 63.09 μm vs. 325.03 ± 56.67 μm, P = 0.002). At 0.5mm, 1.5 mm, and 3.0mm in diameter, the nasal choroidal sectors of the high hypermetropia eyes were significantly thicker than that of the control (P < 0.05). For the choroidal vascular parameters, S.A. values were 1101604.39± 209973.14 μm² in the high hypermetropia eyes and 1072580.21 ± 229841.25μm2 in the control eyes; L.A. values were 2018339.60 ± 324292.51μm2, and 1786624.19 ± 238875.62μm2 in the two groups, respectively; TCA were 3112626.91 ± 521392.85μm2 and 2859204.39 ± 442897.88μm2 in the two groups. L.A. and TCA of the high hypermetropia eyes were significantly larger than that of the normal controls (P = 0.037, P = 0.002). The CVI differed significantly in the two groups (P = 0.001).

Conclusion: The thicker choroidal thickness, rather than topographic features, is a biomarker of high hyperopia, but CVI is another more robust indicator.

Choroidal thickness

Choroidal vascularity index

High hypermetropia

Enhance depth imaging- optical coherence tomography

Clinical significance: we need an accurate method to evaluate the severity of hyperopia

By birth, human beings are predominantly hyperopic, and as the age progresses, hyperopic eyeballs grow to become emmetropic or even myopic^1–5. For children with refractive errors, the most common type is hyperopia worldly. If left untreated, the hyperopia, especially moderate-to-high hyperopia, may develop a series of sequelae, such as amblyopia and strabismus^6–9. Therefore, early diagnosis and severity stratification of hyperopia is vital for physicians to select appropriate management strategies, thus minimizing relevant sequelae.

Current status: current parameters and limitations

The choroid comprises blood vessels, melanocytes, fibroblasts, resident immunocompetent cells, and supporting collagenous and elastic connective tissue. It plays a vital role in ocular physiology by oxygenating and nourishing avascular outer retinal layers, particularly photoreceptors and the optic nerve pre-laminar section of the optic nerve¹⁰. It is reported that the choroid may play an essential role in the visually guided regulation of eye growth and the development of myopia and hyperopia ^1–5, so several choroid-related parameters have been investigated to evaluate the severity degree of hyperopia. Choroidal thickness (CT) is widely used in the evaluation of choroid status, and its value is associated with a range of factors, including age, gender, and refractive errors^11–16. However, CT provides limited information related to the choroid's subtle structural changes.

Problems: C.T. could not measure the subtle changes of hyperopia, but CVI might be

As we know, in the pathological changes of hyperopia, the choroidal thinning associated with myopic axial elongation is primarily the result of reduced thickness of the stromal rather than the vascular component of the choroid¹⁸, so we need the parameters to provide more subtle structural changes, which are not available in C.T.

The rationale of CVI: OCT presents the subtle vascular structures which are related to hyperopia.

With the development of optical coherence tomography (OCT), the measurement of subtle choroid structures becomes possible. Recently, a new quantitative index, choroidal vascularity index (CVI), defined as the ratio of blood vessels' luminal area (L.A.) to the total choroidal area (TCA), has been developed to evaluate the vascular structure of the choroid¹⁷. As CVI, which mainly measures choroidal vascularity, may play a more important role in evaluating hyperopia severity. Most of the previous studies focused on using the CVI to assess the subtle choroid structural changes related to myopia or high myopia. Still, its applications in children with high hyperopia have not been fully documented, especially in the Chinese pediatric population.

Aim of the study

In this study, we used the Enhanced depth imaging – (EDI-OCT) to measure the choroidal thickness and CVI metrics in Chinese children with high hypermetropia and normal controls. We aimed to determine the value of CVI as a characteristic parameter to evaluate the severity of hypermetropia.

Study population

The Institutional Review Board of our hospital approved this observational cross-sectional study, and written informed consent were obtained from all participants.

The participants were consecutively recruited in the Department of Pediatric Ophthalmology of our hospital from June 2021 to September 2021. The inclusion criteria were (1) age between 4 and 14 years, (2) best-corrected visual acuity (BCVA) ≥ 0.8, (3) intraocular pressure (IOP) < 21 mmHg, (4) normal anterior chamber angles, (5) normal optic nerve head (ONH) without glaucomatous changes, such as the neuro-retinal rim narrowing, cup-disc ratio increasing, and no retinal nerve fiber layer abnormalities. The participants with the following criteria were excluded, (1) history of ocular or systemic diseases, including congenital cataract and glaucoma, hypertension, and diabetes, (2) previous intraocular or refractive surgery, (3) neurologic disease, or (4) other evidence of retinal pathology. The demographic data of all enrolled patients were collected for analysis.

Ophthalmologic examinations

All participants underwent comprehensive ophthalmic examinations to collect the following data, which were BCVA, spherical equivalent (D) to evaluate the cycloplegic refraction, slit-lamp biomicroscopy (xx), axial length (mm) (IOL Master; Carl Zeiss Meditec, Dublin, CA), corneal curvature (mm), and IOP (mmHg). Retinoscopy measurements were performed under the cycloplegia, and xx (xx) was collected.

EDI-OCT examinations of retinal and choroidal thickness

The macula was scanned using spectral-domain EDI-OCT (Spectralis, Heidelberg Engineering, Heidelberg, Germany) by one ophthalmologist with ten years of experience in OCT exam throughout the study to measure the choroidal thickness (C.T.) and choroid vascular parameters.

The macular C.T. was measured from the outer portion of the hyper-reflective line corresponding to the retinal pigment epithelium (RPE) to the inner surface of the sclera. The CT measurements were obtained at seven spots along with the macular layer, including directly beneath the fovea or the sub-foveal area (SFCT) point, the temporal and nasal points at a radius of 0.5-mm, 1.5-mm, and 3-mm(Fig. 1).

Image binarization and choroidal vascularity index

Choroid vascular parameters were measured using the Niblack auto local threshold tool in the Image J platform (version 1.47, National Institutes of Health, Bethesda, MD, USA; http://imagej.nih.gov/ij/). Each segmented B-scan through the fovea on OCT was binarized with dark and light pixels to signify the luminal area (L.A.) and stromal area (S.A.) of the choroid, respectively(Fig. 2) The TCA was calculated by multiplying the standard width of 3000 µm (1500 µm on the nasal and temporal side of the fovea) by the center choroidal thickness. Finally, TCA, LA, and S.A. were measured, followed by the CVI, defined as the ratio of L.A. to TCA.

Statistical analysis

The Kolmogorov-Smirnov test was used to analyze the normality of distribution. Descriptive statistics were calculated as the mean and standard deviation for normally distributed variables and median and interquartile range (IQR) for non-normally distributed variables. The independent t-test for normal distributions and Kruskal-Wallis tests for non-normal distributions were used to compare other parameters between groups. The categorical data were described as frequencies and percentages and compared between groups using Fisher's exact test as appropriate. The Tamhane's T2 test was performed to adjust for multiple comparisons between groups within each analysis. A two-sided P value less than 0.05 was considered statistically significant. Statistical analysis was performed using the SPSS software version 21 (SPSS, Inc., IL, USA).

Measures of central tendency in continuous data were described as median (or mean) and range, and categorical data were described as frequencies and percentages. The propensity score matching method was used to match the control cases with patients with complications. The continuous variables were compared using a t-test, and the ordinal variables were compared using conditional logistic regression. P < 0.05 was considered statistically significant.

Patients and baseline data

In the study interval, a total of 50 children were enrolled, including 21 with high hypermetropia (female/male = 10/11, age 5.31 ± 1.69 years) and 29 normal controls (female/male = 14/15, age 6.36 ± 1.22 years) (Table 1). The patients were classified according to spherical equivalent (S.E.), which were high hyperopia with S.E. of + 5.00D or more, and normal controls with S.E. of -0.50D ~ + 1.00D.

Table 1

Demographic and Clinical Characteristics of Enrolled Patients (n = 50)
	High hypermetropia group	Normal control group	P value
Number of eyes (n)	41	29	-
Age (year)	5.31 ± 1.69	6.36 ± 1.22	-
Gender (male/female)	11/10	15/14	P = 0.812
Spherical equivalent (D)	+ 5.71 ± 1.99	0.24 ± 0.07	P < 0.001
BCVA	0.06 ± 0.09	-0.01 ± 0.06	P = 0.532
IOP (mmHg)	16.85 ± 3.44	15.19 ± 6.14	P = 0.574
Axial length (mm)	20.85 ± 0. 89	23.85 ± 0..67	P < 0.001
Corneal curvature (mm)	8.02 ± 1.91	7.92 ± 1.69	P = 0.174
BCVA, best corrected visual acuity; SD, standard deviation; D, diopter; logMAR, minimal angle of logarithm.

The demographic and ocular characteristics were listed in the study (Table 1). Significant differences were observed on spherical equivalent (+ 5.71 ± 1.99D vs. 0.24 ± 0.07D, P < 0.001) and AL (20.85 ± 8.91mm vs. 23.85 ± 6.69 mm, P < 0.001) between the two groups was observed (P = 0.812), while no differences were found on other parameters.

Choroidal parameters measured by OCT

The sub-foveal choroidal thickness (SFCT) was significantly thicker in the high hypermetropia eyes than that in normal controls (371.32 ± 63.09 µm vs. 325.03 ± 56.67 µm, P = 0.002) (Table 2). At 0.5mm, 1.5 mm, and 3.0mm in diameter, the nasal choroidal sectors of the high hypermetropia eyes were significantly thicker than that of the normal control eyes (P < 0.05). For the 0.5 mm sector, the temporal C.T. was significantly thicker in high hypermetropia eyes than that in normal control eyes (362.27 ± 57.45 µm vs. 325.07 ± 50.23 µm, P = 0.006).

Table 2

Sub-foveal retinal and choroidal characteristics
	High hypermetropia group (n = 21), mean ± SD	Normal control group (n = 29), mean ± SD	P value
CT* (um)
Sub-foveal	371.32 ± 63.09	325.03 ± 56.67	P = 0.002
Nasal 0.5	361.39 ± 60.58	314.41 ± 53.43	P = 0.001
Nasal 1.5	335.07 ± 53.90	254.17 ± 55.24	P < 0.001
Nasal 3.0	246.15 ± 55.67	166.83 ± 39.68	P < 0.001
Temporal 0.5	362.27 ± 57.45	325.07 ± 50.23	P = 0.006
Temporal 1.5	340.83 ± 50.86	317.76 ± 48.52	P = 0.061
Temporal 3.0	309.88 ± 61.19	298.86 ± 49.37	P = 0.425
Choroid vascular parameters
TCA in mm²	3112626.91 ± 521392.85	2859204.39 ± 442897.88	P = 0.037
LA in mm²	2018339.60 ± 324292.51	1786624.19 ± 238875.62	P = 0.002
SA in mm²	1101604.39 ± 209973.14	1072580.21 ± 229841.25	P = 0.586
CVI (LA/TCA)	0.65 ± 0.02	0.63 ± 0.03	P = 0.001
CT, choroidal thickness; CVI, choroidal vascularity index; SA, stromal area; LA, luminal area; TCA, total choroidal area

For the choroidal vascular parameters, S.A. values were 1101604.39 ± 209973.14 um² in the high hypermetropia eyes and 1072580.21 ± 229841.25 µm² in the control eyes (Table 2); L.A. values were 2018339.60 ± 324292.51 µm², and 1786624.19 ± 238875.62 µm² in the two groups, respectively; TCA values were 3112626.91 ± 521392.85 µm² and 2859204.39 ± 442897.88 µm² in the two groups. L.A. and TCA values of the high hypermetropia eyes were significantly larger than that of the normal control eyes (P = 0.037, P = 0.002, respectively). The CVI values differed significantly in the two groups (P = 0.001).

Relationship between choroidal parameters and their potential impact factors

Correlation analysis were performed between the choroidal parameters and age, AL, and sphere (Table 3). Our results showed that age was significantly correlated with AL (r = 0.324, P = 0.006), SFCT (r = -0.286, P = 0.016), LA (r = -0.242, P = 0.043), SA (r = -0.262, P = 0.029) and TCA (r = -0.255, P = 0.033), while no correlation with CVI (r = 0.058, P = 0.631) was found. The AL was significantly correlated with SFCT (r = − 0.522, P < 0.001), LA (r = -0.530, P < 0.001), SA (r = -0.291, P = 0.015) and TCA (r = -0.451, P < 0.001), but not the CVI (r = − 0.219, P = 0.069). Sphere was found to be significantly correlated with AL (r = -0.897, P < 0.001), SFCT (r = 0.302, P = 0.011), LA (r = 0.311, P = 0.009) and CVI (r = 0.335, P = 0.005), whereas no significant association between SA and TCA (P = 0.745, 0.086, respectively).

Table 3

Correlation between choroid microstructure parameters and other baseline parameters in all patients (n = 50)
Parameters	AL		SFCT		LA		SA		TCA		CVI
Parameters	r	P	r	P	r	P	r	P	r	P	r	P
Age	0.324	0.006	-0.286	0.016	-0.242	0.043	-0.262	0.029	-0.255	0.033	0.058	0.631
AL	-	-	-0.522	0.000	-0.530	0.000	-0.291	0.015	-0.451	0.000	-0.219	0.069
Sphere	-0.897	0.000	0.302	0.011	0.311	0.009	0.040	0.745	0.206	0.086	0.335	0.005
AL, Axial length; SFCT, sub-foveal choroidal thickness S.A., stromal area; L.A., luminal area; TCA, total choroidal area; CVI, Choroidal vascularity index.

This study has provided a comprehensive assessment of the topographical variations in choroidal thickness, including the luminal and stromal area and choroidal vascularity index in Chinese children with high hypermetropia.

Choroidal thickness is different between the two groups and the significantly higher in the high hyperopia group. A significant difference was found in the following spots, including sub-foveal, Nasal 0.5, Nasal 1.5, Nasal 3.0, Temporal 0.5

Choroidal thickness is the main parameter used to obtain information about the choroidal layer and has been examined in children and adolescents in many studies^19–22. In healthy pediatric populations, the mean sub-foveal from these studies ranged from 245 to 361 µm^20–22. Read et al.²³ reported that the mean of the sub-foveal choroidal thickness of 330 ± 65 um in Australian children (4 ~ 12 years) with spherical equivalent refractive errors (SER) (+ 1.25 ~- 0.50 D). Takafumi Mori and Yukinori Sugano also found a similar result in preschool Japanese children²⁴. Additionally, Zha Yi et al.²⁵ reported that the sub-foveal choroidal thickness of 328.12 ± 65.93µm in 4–12 years old Chinese children with SER was between − 1.75D to + 0.63D. Our study in normal children had very close values (325.03 ± 56.67 µm)for age-matched normal children. Our results support that variations of choroidal thickness measurements for normal children between studies might result from age, ethnic differences, and different measurement techniques.

The value of choroidal thickness in evaluating the degree of refractive errors or amblyopia had also been depicted in some studies^{19, 24–26}. The results are roughly the same in different cohorts: the myopic eyes had thinner sub-foveal choroidal thickness, and the hyperopic eyes and hyperopic amblyopic eyes had thicker choroidal thickness than emmetropic eyes and myopic eyes. However, few studies focused on the structural characteristic of the choroid in high hyperopia subjects. In the current study, both the subfoveal choroidal thickness and topographical variation in high hyperopic children were described. Consistent with the existing conclusions, we found that the sub-foveal choroidal thickness in high hyperopia children was significantly thicker than that in the emmetropic control group. The average choroidal thickness in the hyperopia group in our study was similar to the results of previous studies, but they seemed to be lower than those in the hyperopic amblyopia children with lower SER, which might verify the previous speculation that hyperopia was associated with subfoveal ChT, whereas amblyopia had no significant independent effect on subfoveal ChT in our study population²⁵. The pathophysiologic mechanisms involved need further verification. Additionally, the topographic features of the choroid in the hyperopia group in this study were almost the same as those in controls: the choroid was the thickest in the sub-foveal region and the thinnest in nasal regions which approach the optic nerve(Fig. 3). These findings were also consistent with previous results of children either with different refractive status or with amblyopia, indicating the relatively stable choroid contour in pediatric populations^{19, 25}.

In normal eyes, choroidal thickness in children can be affected by various factors, such as age, gender, diopter, and axial length. Previous studies reported a significant association between the A.L. and choroidal thickness^27–29. Nagasawa et al. and Bidaut-Garnier reported that ChT was negatively correlated with axial length^{30, 31}. Li et al. reported that a thinner subfoveal choroidal thickness correlated with a longer A.L. but no other factors, such as age, sex, and SER in myopic children³². Read et al. found that choroidal thickness increased in children with normal axial elongation, whereas children undergoing faster A.L. elongation tended to exhibit less thickening and a thinning of the choroid in some cases³³. In the current study, a thinner SFCT was also found to be negatively correlated with longer A.L. and larger age but positively correlated with the sphere in normal and hyperopic children. However, the causal relationship between choroidal thickening and hyperopia remains controversial.

Since CT could be affected by sorts of variables and could not represent the choroid's subtle structural changes, we cannot assess the choroid structural changes and blood supply only by C.T. measurement. Recently, Agrawal et al.¹⁷ assessed the L.A., S.A., and TCA through EDI-OCT images and proposed a new parameter- CVI to assess the choroidal vascular structure. In their study, they found that CVI was less affected than the sub-foveal choroidal thickness and suggested CVI be a more robust marker of choroidal diseases. Subsequently, other studies have also demonstrated less variability of CVI. In our study, we found that the A.L. was significantly correlated with SFCT but not the CVI, which was consistent with the previous results, further indicating that CVI might be an alternative metric for the evaluation of choroidal disorders.

On the other hand, a shorter A.L. tended to be associated with a bigger L.A., S.A., and TCA. Li et al. reported that changes in luminal areas might directly influence choroidal thickness, as blood vessels represent the main component of the choroid³². Meryem et al.³⁴ found that TCA and S.A. were higher in hyperopia than in both emmetropic and myopic eyes. In the present study, L.A. and TCA values and CVI of the high hypermetropia eyes were significantly larger than that of the normal control eyes suggesting an increase in blood flow and blood vessel area in eyes with shorter A.L.s. It is still unknown whether the thickening of the choroid in hyperopia is caused by the increase of stromal area or the enlargement of the vascular luminal area. Multi-center studies with large sample sizes are needed for further validation.

Age is also an important factor affecting choroid structure. Previous studies found that the choroidal thickness tended to decrease with increasing age in adults^{27, 28} Fujiwara et al. found that choroidal vascular density had a negative association with age in healthy adults³⁵. Ruiz-Medrano et al.³⁶ found that the choroidal stromal area was not affected by age in a healthy population that included normal children. In our study, stromal area, luminal area, and total choroidal area were found to decrease significantly with increasing age.

Our study has several limitations. First, the sample size is relatively small, and the high hyperopes are all Chinese children. Second, the OCT measurement of each subject in our study was performed at a randomized time at their convenience. Further studies with a large population and unified examination time are needed for more positive and robust results.

In summary, to our knowledge, the current study provides the first description of the structural features of the choroid and the factors influencing them in Chinese children with high hyperopia. We suggest that thicker choroidal thickness, rather than topographic features, is a biomarker of high hyperopia, but CVI is another more robust indicator.

AL: Axial length; BCVA: best-corrected visual acuity; IOP: Intraocular pressure; LogMAR: logarithm of the minimum angle of resolution; CT： Choroidal thickness； TCA： total choroidal area； S.A.， stromal area； L.A.， the luminal area； CVI， The Choroidal vascularity index； EDI-OCT： Enhance depth imaging- optical coherence tomography

Acknowledgments

Not applicable.

Funding

Not applicable.

Availability of data and materials

The data that support the findings of this study are available from the corresponding author on reasonable request.

Authors’ contributions

DHZ and H.W. were responsible for the study design. RS L, J.W., RY L and JJ Z examined all subjects. H.W. collected the data. H.W. and RSL contributed to the data analysis. DHZ made major contributions to writing the manuscript. DHZ revised and edited the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

This study was approved by the Ethics Committee of Peking University First Hospital and complied with the Declaration of Helsinki. Written informed consent was obtained from a parent or guardian for participants under 16 years old.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

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Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author Details

Department of Pediatric Ophthalmology, Peking University First Hospital Peking university Peadatriac vision research Center, No.8 Xishiku Street, Xicheng District, Beijing 100034, China

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No competing interests reported.

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Choroidal thickness and vascularity index in Chinese children with high hypermetropia using optical coherence tomography (OCT)

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Abstract

Figures

Background

Clinical significance: we need an accurate method to evaluate the severity of hyperopia

Current status: current parameters and limitations

Problems: C.T. could not measure the subtle changes of hyperopia, but CVI might be

The rationale of CVI: OCT presents the subtle vascular structures which are related to hyperopia.

Aim of the study

Methods

Study population

Ophthalmologic examinations

EDI-OCT examinations of retinal and choroidal thickness

Image binarization and choroidal vascularity index

Statistical analysis

Results

Patients and baseline data

Choroidal parameters measured by OCT

Relationship between choroidal parameters and their potential impact factors

Discussion

Conclusion

Abbreviations

Declarations

References

Additional Declarations

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