South African Eye Study: Establishing a normative database for retinal nerve fibre layer thickness in a black ethnicity paediatric population

doi:10.21203/rs.3.rs-4127244/v1

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South African Eye Study: Establishing a normative database for retinal nerve fibre layer thickness in a black ethnicity paediatric population

https://doi.org/10.21203/rs.3.rs-4127244/v1

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Background:

The retinal nerve fibre layer (RNFL) thickness in South African children of black ethnicity is not known. Current imaging devices do not include a paediatric normative database. There is also a lack of data on global majority ethnicities. This study used spectral-domain optical coherence tomography (SD-OCT) to describe the average and quadrant RNFL thickness in children of black ethnicity.

Methods: A prospective cross-sectional hospital-based study was conducted at McCord Provincial Eye Hospital, Durban, South Africa, with a convenience-based sampling strategy. One normal eye from children between the ages of 5 and 18 were selected. An ocular examination included an autorefraction and an axial length measurement. The RNFL thickness was measured with the iVue-100 SD-OCT™.

Results:Seventy-three children were enrolled in this study based on power calculations. The mean (standard deviation) average RNFL thickness was 107.31um (8.1). The mean (standard deviation) inferior, superior, nasal, and temporal quadrant thickness were as follows: 135.1um (13.65), 135.6um (14.59), 83.2um (10.86), and 75.4um (9.03). No correlation was found between the average RNFL thickness and age, sex, spherical equivalent, and axial length with a p-value of 0.438, 0.106, 0.632, and 0.20 respectively.

Conclusion: This study described the normative values for retinal nerve fibre layer thickness using SD-OCT in South African children of black ethnicity between 5 and 18 years old and supports paediatric ethnic variation in the RNFL thickness. Establishing a normative database could help screen, diagnose and monitor glaucoma and other optic nerve pathologies in this paediatric ethnic group.

Health sciences/Anatomy

Health sciences/Diseases/Eye diseases/Optic nerve diseases

Health sciences/Health care/Paediatrics

The African continent is the second largest and second most populous in the world, home to 1.46 billion people of diverse ethnicities, with a reported 41% of the population being under the age of 15 years (1). Globally, there are significant populations of African ancestry. Brazil has the highest African diaspora population, estimated at 55.9 million, followed by the United States with 46.4 million (13.6% of the population) people of African descent (2). Despite this, there is a paucity of research on establishing normative databases on the RNFL thickness for this population, most especially within the paediatric sub-group.

The current estimated global population of primary open-angle glaucoma is 68.56 million. Africa has the highest prevalence (4%) of all continents, according to a recent 20-year meta-analysis (3). A South African meta-analysis from 2010–2020 showed prevalence estimates of blindness of 2% and moderate and severe visual loss of 12% with glaucoma accounting for 17% and 7% respectively (4).

The prevalence of juvenile glaucoma in South Africa is unknown. It is reported that glaucoma is the cause of visual impairment in about 6.7% of children in South African Blind schools (5).

Diagnosing glaucoma in children is challenging. Obtaining reliable visual fields and intraocular pressures requires understanding and cooperation. This is difficult, especially in younger children. Optic nerve head assessment is subjective amongst ophthalmologists, and in certain cases, it is challenging to differentiate physiological cupping from glaucomatous cupping.

Scanning the optic nerve head with spectral-domain optical coherence tomography (SD-OCT) provides an objective measure of the retinal nerve fibre layer (RNFL) thickness. This imaging device is non-invasive with good reproducibility in the paediatric population (6, 7). Establishing geographical and ethnic-specific normative data will help to achieve more accurate clinical risk stratification and prognostication for glaucoma screening, monitoring, and management (8). There are no age-matched normative RNFL thickness data for children under 18 years old in OCT devices; therefore, using initial visit scans as a baseline is often the only way to monitor progressive RNFL thinning.

There are currently no studies on the RNFL thickness in South African children of black ethnicity. In the whole of Africa, there is only one study in Kenya that investigated the RNFL thickness in children of black ethnicity (9). Ethnic differences in the RNFL thickness have been reported in children; however, limited data exist. In North Carolina, children of black ethnicity were reported to have a thicker average RNFL (110.7um) when compared to children of white ethnicity (105.9um) (10). Children of East Asian descent had a thicker RNFL (105.45um and 107.92um) when compared to children of European Caucasian descent (101.95um and 104.57um) in 6 and 12-year-olds, respectively (11). Apart from the lack of a paediatric normative database in OCT devices, there are ethnic variations in the RNFL thickness in children that need to be considered.

We are currently using OCT devices with adult normative databases to diagnose glaucoma in children, and these databases are also not representative of our black ethnic population of 80.9% (12). The iVue100™ SD-OCT normative database has an African descent representation of 10% (13). The Cirrus™ HD-OCT normative database has an African-American representation of 18% (14). The Spectralis™ SD-OCT has a Caucasian normative database (15). In South Africa, these are the common OCT devices used in our daily clinical practice. We rely on these objective measurements as part of evaluating and managing glaucoma in our children.

In addition to establishing a paediatric OCT RNFL normative database to help screen, diagnose, and monitor juvenile glaucoma, OCT is being increasingly utilized as an objective clinical tool in other paediatric optic neuropathies such as optic neuritis and compressive optic neuropathies.

Our study aimed to describe normative values for retinal nerve fibre layer thickness using SD-OCT in South African children of black ethnicity between 5 to 18 years old.

A cross-sectional hospital-based study at McCord Provincial Eye Hospital (MPEH), Durban, South Africa, from September 2020 to July 2023, involved children of black ethnicity between 5 to 18 years old.

Patient recruitment began once ethical approval was obtained from the Biomedical Ethics Review Committee of the University of KwaZulu-Natal (BREC/00001374/2020). This study adhered to the tenets of the Declaration of Helsinki and good clinical practice.

A convenient sample method was used where patients were included consecutively as they met the inclusion criteria. The parent or legal guardian who self-identified as black ethnicity signed consent for voluntary participation and assent was assessed by the child’s willingness to cooperate.

Children were included if they met the following criteria:

one normal eye (only one eye included for each child)
best corrected visual acuity of 6/9
normal anterior and posterior segment
normal intraocular pressure
children with strabismus or mild allergic conjunctivitis (mild conjunctival injection or papillae and no corneal involvement) on topical olopatadine and intermittent use of fluorometholone 0.1% for acute flare-ups were included since these were common presenting problems of this age group at MPEH.

Children were excluded as follows:

systemic medical disease
family history of glaucoma
previous intraocular surgery or laser
born less than 37 weeks postmenstrual age
history of retinopathy of prematurity
previous trauma to the eye
chronic use of topical steroids
IOP ˃ 21mmHg
vertical cup-disc ratio ˃ 0.6 or any optic nerve that looked suspicious for glaucoma
cup-disc asymmetry of ˃ 0.2
hypermetropia ˃ + 3.00D
myopia ˃ -5.00D
astigmatism ˃2.00D
axial length ˂ 22mm or ˃ 25mm
uncooperative children

Visual acuity was measured using a 6m Snellen chart and converted to decimal notation. Intraocular pressure was measured with the iCare IC100™ tonometer (North Carolina, icare USA, inc.). A slit lamp examination of the anterior and posterior segments was performed on all patients by the investigator.

Children with strabismus were required to have a cycloplegic refraction to exclude high hyperopia. All other children had an autorefraction (NIDEK ARK-1, NIDEK CO., LTD, Japan) or a subjective refraction by the optometrist. The spherical equivalent was calculated as the spherical power plus half of the cylindrical power value.

Axial length was measured using the ZEISS IOL master 500 (Carl Zeiss Meditech, Germany). Tropicamide 0.5% was used to dilate the pupil if the fundus examination was difficult.

The RNFL thickness was measured using the iVue100™ SD-OCT (Optovue Inc, Fremont, CA, USA, software version 2018.1.1.60) optic nerve head protocol. The child was asked to look at the green fixation cross in the machine, and the investigator observed and centered the aiming circle on the optic disc. The RNFL was measured along this circle of 3.45mm diameter. A green highlighted Scan Quality Index (SQI > 27) indicated a good quality scan. The inferior, superior, nasal, temporal, and average RNFL thickness were recorded. Our data collection sheet included an interviewer-administered questionnaire in the context of exclusion factors. All data was then transferred to an Excel spreadsheet.

A sample size of seventy-three was required to estimate the retinal nerve fibre layer to within 3 microns (medium effect size of 0.3) with a probability of 95% and a baseline estimate of 99 +/- 9um using previous studies as a guide. A statistician and the primary author used Stata statistical analysis to calculate the sample size.

Statistical analysis

Statistical analysis was done using Jamovi (The Jamovi Project, version 2.4, 2022) and R (R Core Team, 2022). Analysis of variance (ANOVA) between groups was performed in all quadrants as well as average RNFL thicknesses. Descriptive statistics such as ranges, means, standard deviations, and confidence intervals were used to determine the main outcome parameters. A 2-tailed Pearson bivariate correlation matrix was used to determine the associations between RNFL thickness and ordinal and continuous risk profile parameters. Independent samples t-test was used for associations to categorical variables. All p-values were two-sided, and a probability (p-value) < 0.05 was considered statistically significant.

Seventy-three children were included in this study. The demographics and ocular parameters are shown in Table 1.

The average retinal nerve fibre layer thickness had a mean (standard deviation [SD]) of 107.3um (8.1). Mean (SD) quadrant values were as follows: inferiorly 135.1um (13.65), superiorly 135.6um (14.59), nasally 83.2um (10.86), and temporally 75.4um (9.03).

There was no correlation between the average RNFL and age, sex, spherical equivalent, and axial length with a p-value of 0.438, 0.106, 0.632, and 0.20, respectively.

There was a good distribution of males and females over this sample and a relatively equal representation of right and left eyes. The mean (SD) age of 10.1 (2.8) represents an age group more likely to understand and cooperate for eye examinations. Selection bias likely accounted for the narrow range of refractive errors that were included.

Our study found a mean (SD) average RNFL thickness of 107.31um (8.1). The superior and inferior quadrants were the thickest, with almost similar values (135.6um and 135.1um respectively), followed by the nasal (83.2um) and temporal quadrants (75.4um). Our results followed the “double hump pattern”, which represents a normal pattern where the superior and inferior quadrants are thicker (16).

The RNFL thickness distribution did not follow the “ISNT rule” where the inferior quadrant is the thickest followed by the superior quadrant; however, variability in the distribution of the RNFL thickness has been shown in a systematic review of RNFL normative data in children. Deviation from the “ISNT rule” may not always infer pathology. There is variability in the average and quadrant RNFL thickness even amongst normal children. The average RNFL thickness ranged from 92–117.3um in this systematic review that included 74 studies of varying methodologies and OCT devices and comparisons are therefore not feasible (17).

Commercially available OCT devices use different scanning patterns to measure this layer. The RNFL thickness is calculated as the distance from the internal limiting membrane to the outer limits of the RNFL. Most OCT devices calculate the RNFL thickness along a circle of predefined diameter (usually between 3.4 and 3.5mm) centered on the optic disc. One of the reasons OCT devices cannot be used interchangeably is the RNFL measurement along circles of different diameters (16). Various inter-and intraoperator agreements exist amongst different OCT devices (18). OCT devices have a similar ability to detect glaucoma. However, different acquisition rates, resolution, and RNFL detection algorithms are different in each device and should not be used interchangeably (19, 20).

The RNFL thickness can also be affected by age, sex, axial length, refractive error, and ethnicity.

There was no correlation between the RNFL thickness and age in our study, and other studies had similar findings; however, we did not have a good representation of each age group (21, 22, 23, 24, 25). A population-based study by Li Chen et al. reported that in children older than 11 years, the RNFL thickness decreased significantly with age (26).

In our study, male children had a slightly thicker mean (SD) average RNFL (109um [8.52]) when compared to female children (106um [7.41]); however, this was not statistically significant (p-value 0.106). Our findings were supported by a systematic review, which stated that RNFL is not influenced by sex in the paediatric population (17).

A normal range of axial length and a narrow range of refractive errors were selected; therefore, we did not expect a correlation with the RNFL thickness. This was also found in a study by Turk et al., which included a normal range of axial length and a narrow range of refractive errors (-0.27 ± 0.99D) (21).

Axial length and refractive error can affect the RNFL thickness, with a thicker RNFL reported in hyperopic children and a thinner RNFL in myopic children. Studies report that ocular magnification associated with the axial length and refractive error is attributed to the changes in the RNFL thickness seen in myopes and hyperopes, and these differences disappear after applying the Litmann formula (27, 28, 29, 30).

There are no studies published on the RNFL thickness in South African children for comparison. The single Kenyan study that investigated the RNFL thickness reported the RNFL thickness in 128 Kenyan children and compared the findings to 130 children from Bhutan (Asia). The mean age (SD) was 6.4 (1.5), and the average (SD) RNFL thickness in Kenyan and Bhutanese children in the right eye was 108.3um (10) using the iScan™ OCT device (Optovue Inc). There was no statistical difference found between the two groups (9).

We compared our data to a population-based study by Li Chen et al. on an Asian paediatric population between the ages of 6–17. The study included 4648 eyes of 2324 Chinese students, and the RNFL thickness was scanned using the iVue100™ SD-OCT (26). Our study had a small sample size, however, with a similar methodology. The average RNFL thickness in both groups was similar (106.89um and 107.32um). South African children of black ethnicity had thicker inferior and nasal quadrants (p < 0.001), and Chinese children had a thicker temporal quadrant (p < 0.001) (Table 2). This finding, together with the above-mentioned Kenyan study, may imply a similar average RNFL thickness in children of African and Asian descent.

Research outside Africa that included children of black ethnicity is also limited. Most paediatric studies on RNFL normative databases included mostly Caucasian and Asian ethnic groups (17). Yanni et al. reported the RNFL thickness in 83 children from North America using the Spectralis™ SD-OCT. The average RNFL thickness was 107.6um, which included only 5 African-American children, with non-Hispanic white ethnicity being the majority ethnic group (23). El-Dairi et al. reported a thicker RNFL in children of black ethnicity compared to children of white ethnicity (110.7um versus 105.9um) from North Carolina using the Stratus OCT-3™ (Carl Zeiss Meditec). The study included 114 children of black ethnicity and 154 children of white ethnicity with a mean (SD) age of 8.5 (3.1) (10).

Our sample of children had a statistically significant thicker average (107.32um versus 103.9um), superior, and inferior quadrant RNFL when compared to a Caucasian ethnic paediatric population in Turkey (Table 3). This study by Kiziloglu O, Yabas et al. investigated the RNFL thickness of 202 children between the ages of 5 to 17 using the iVue100™ SD-OCT. The mean age (SD) of 10.4 (3.4) was similar to our study. This finding supports an ethnic variation of the RNFL in children and implies that children of black ethnicity have thicker RNFL when compared to children of Caucasian ethnicity.

Comparative studies of the RNFL thickness between children and adults are poorly documented. Our children had a similar average RNFL when compared to our adult population of black ethnicity (107.32um and 106.97um), with children having a thicker superior quadrant (p = 0.008) and adults having a thicker nasal quadrant (p = 0.013) (Table 4). This study by Mashige et al. included 600 participants with a mean (SD) age of 28.15 (13.09) and an age range of 10–60. The iVue100™ SD-OCT was used, and the mean average RNFL thickness was reported as 110.01um. An average RNFL value of 106.97um was recalculated by summating the reported quadrant values. The number of children included in this study was not reported (31).

Ismail et al. have shown that South African adults of black ethnicity have a thicker global RNFL (108.7um) when compared to the European database (97.1um) on the Spectralis™ SD-OCT.

We compared our data to this study, taking into consideration that a different OCT device was used. Our children had an average RNFL thickness of 107.32um, which may suggest that children of black ethnicity also have a thicker RNFL than the European database on the Spectralis™ SD-OCT. Adults had thicker superior quadrants (p = 0.017), and children had thicker nasal quadrants (p = 0.005) (Table 5) (32).

Despite the higher prevalence of glaucoma and poorer visual outcomes in individuals of African descent, studies establishing normative databases in Africa are few. In Ghana, West Africa, the prevalence of primary open-angle glaucoma is 8.5%, which is reported to be the highest in Africa and second in the world. The average RNFL thickness in a normal Ghanaian black ethnic population is 102.37um (Cirrus™ HD-OCT 500) (33). In normal Nigerian adults, the RNFL thickness was 104.17um (Stratus OCT™, Carl Zeiss Meditech) (34).

African-American adults were reported to be at a higher risk of developing glaucoma. The Baltimore Eye survey reported that the prevalence rates of primary open-angle glaucoma were 4–5 times higher in black ethnic individuals compared to white ethnic individuals (35). In a population-based multiethnic study, African-American adults had an average value of 90.87um and were reported to have the thinnest RNFL thickness compared to Latino Americans and Chinese Americans (Cirrus™ HD-OCT 4000) (36).

Both South African studies on adults of black ethnicity report higher values than adults of black ethnicity in other African countries, African Americans, as well as other ethnic groups, including Indian, Nepalese, and Brazilian individuals (31, 32).

The application of OCT in other paediatric optic neuropathies as an objective measure of the RNFL thickness can help determine disease severity and visual prognosis. Optic neuritis can occur as part of a Relapsing Demyelinating Syndrome (RDS) that includes conditions such as multiple sclerosis and aquaporin-4 antibody neuromyelitis optical spectral disorders. The long-term visual impairment in children with RDS is inversely correlated with the RNFL thickness (37). Thinning of the RNFL is related to decreased visual function in conditions such as optic nerve hypoplasia and congenital glaucoma (38, 39). Paediatric tumours such as craniopharyngiomas and pituitary adenomas can cause compression of the optic nerve. This can cause progressive RNFL thinning which can be detected with serial OCT measurements.

Optical coherence tomography can be used as an objective measure of the structure of the optic nerve and indirectly helps us assess visual function in young children. Therefore, a normative, age- and ethnic-specific database is needed to ensure the best representation of the normal distribution of the RNFL.

Strengths and Limitations

Our hospital-based study with a small sample size involved a single ethnic group. Therefore, the results cannot be generalized to other ethnic groups. Information bias, such as self-reported ethnicity and history in the context of exclusion factors, must be considered. Cycloplegic refraction was not performed on all children, and hyperopia may have been missed. Reche et al. reported no statistically significant differences in RNFL thickness in children with strabismus, and we did not consider this to affect our results (40).

The influence of corticosteroids on raised intraocular pressure is well documented in the literature. A study by Cingu et al. reported a thinner RNFL in children with vernal keratoconjunctivitis on long-term topical corticosteroid use (41). The direct effect of topical corticosteroids and the RNFL thickness needs more research and until strong evidence suggests that topical corticosteroids affect the RNFL, we do not consider short-term use of fluoromethalone 0.1% as a major confounding factor. The association between the retinal nerve fibre layer and allergic conjunctivitis also requires further research as a single study reported a slightly thinner RNFL in Chinese children with allergic conjunctivitis (42). We did not consider the influence of other optic nerve head parameters on the RNFL thickness. There are ethnic differences in optic disc size and cup-disc ratios. African American adults are reported to have larger disc areas and cup-disc ratios (43, 44), and studies have reported a positive correlation between optic disc size and RNFL thickness; however, this is controversial (45, 46).

The investigator performed all clinical examinations and investigations and therefore eliminated inter-observer bias. Study methodologies and different OCT devices and software versions make comparison studies challenging.

Recommendations

Interestingly, our paediatric population had a similar average RNFL with differences in the quadrant values when compared to our adult population of the same ethnicity using the same OCT device. Further research on South African children and adults is required to establish normative databases in our predominantly black ethnic population. This should ideally be a multi-center study with identical protocols.

Research in Africa is neglected and may be partly attributed to a lack of resources, financial support, and other systemic barriers. Current OCT devices do not allow input from local normative databases, and it is the responsibility of the clinician in a resource-constrained environment to be aware of the normative database in their OCT device and to research their own ethnically diverse population for comparison. OCT manufacturers must consider paediatric and ethnic-specific normative databases and allow input of this data into their device to allow for better representation of the normal values of the RNFL across diverse population groups.

Manufacturers of commonly used OCT devices are based outside of Africa, and therefore, African normative database representation is lacking. This population, however, has the highest risk of glaucoma.

This study reports on the normal RNFL thickness in South African children of black ethnicity, supporting ethnic variation in the RNFL thickness.

Paediatric normative databases are needed in OCT devices. This will assist our diagnostic evaluation of children with glaucoma and other optic nerve disorders, which has implications for clinical care and public health. Ethnic-specific normative databases in children and adults are needed to ensure that all groups, including high-risk ethnic groups, are equitably represented. This will make our interpretation of the RNFL thickness more clinically meaningful.

Acknowledgments

Dr. CH. Kruse for support and help with statistical analysis.

Sister P. Bhengu and Dr. M. Mjwara for translating consent and assent forms into isiZulu.

Optometry department for assistance with patient recruitment and refraction.

Author contribution statement:

N. Govender

Designing and writing out protocol.

Conducted research and data collection.

Data analysis, interpretation, and writing of the report.

S. Baboolal

Contributed to the design and writing of the protocol.

Contributed to data analysis and interpretation of results.

Guided writing the report.

Contributed to the writing of the report with multiple reviews and feedback.

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

No financial support required.

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Tables 1 to 5 are available in the Supplementary Files section.

There is no conflict of interest

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South African Eye Study: Establishing a normative database for retinal nerve fibre layer thickness in a black ethnicity paediatric population

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Abstract

Introduction

Materials and Methods

Statistical analysis

Results

Discussion

Strengths and Limitations

Recommendations

Conclusion

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References

Tables

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Supplementary Files

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