Abstract
Purpose
During routine eye examinations, we noticed widened and flattened foveal pits with loss of normal V-shaped foveal profile and a pseudohole-like appearance in some otherwise healthy hypermetropic children. Our purpose was to describe clinical significance and multimodal imaging features of this incidental finding.
Methods
Prospectively, 25 eyes of 13 hypermetropic children with these foveal changes and 36 eyes of 19 hypermetropic children with normal foveal appearance were enrolled. The macular thickness measurements and foveal parameters including pit diameter, depth, base, and area obtained by optical coherence tomography (OCT) (Heidelberg Spectralis, Heidelberg Engineering, Heidelberg, Germany), macular superficial and deep vessel density (VD) and foveal avascular zone values obtained by optical coherence tomography angiography (Avanti RTVue‑XR; Optovue, Fremont, CA, USA) were noted. The correlations of these parameters with visual function were evaluated.
Results
In the study group, significantly widened and flattened pit contours with decreased central foveal thickness (p = 0.01), and increased distance between foveal edges (p < 0.001) were observed. While the whole image superficial macular VD was similar between the groups (p = 0.74), a significant decrease in deep macular VD was observed in the study group (p = 0.01). None of these changes were correlated with visual acuity.
Conclusion
Wider and flattened foveal pits described here represent a newly defined variation in healthy hypermetropic children. Although a correlation with visual acuity was not evident, these changes in foveal profile are shown to be related with macular microvascular changes in deep capillary plexus. Awareness of these morphologic changes will help clinicians in the differential diagnosis of macular pseudohole.
Similar content being viewed by others
References
Hirsch J, Curcio CA (1989) The spatial resolution capacity of human foveal retina. Vision Res 29:1095–1101. https://doi.org/10.1016/0042-6989(89)90058-8
Rossi EA, Roorda A (2010) The relationship between visual resolution and cone spacing in the human fovea. Nat Neurosci 13:156–157. https://doi.org/10.1038/nn.2465
Tick S, Rossant F, Ghorbel I, Gaudric A, Sahel JA, Chaumet-Riffaud P, Paques M (2011) Foveal shape and structure in a normal population. Invest Ophthalmol Vis Sci 52:5105–5110. https://doi.org/10.1167/iovs.10-7005
Dubis AM, Hansen BR, Cooper RF, Beringer J, Dubra A, Carroll J (2012) Relationship between the foveal avascular zone and foveal pit morphology. Invest Ophthalmol Vis Sci 53:1628–1636. https://doi.org/10.1167/iovs.11-8488
Yuodelis C, Hendrickson A (1986) A qualitative and quantitative analysis of the human fovea during development. Vision Res 26:847–855. https://doi.org/10.1016/0042-6989(86)90143-4
Hendrickson A, Possin D, Vajzovic L, Toth CA (2012) Histologic development of the human fovea from midgestation to maturity. Am J Ophthalmol. https://doi.org/10.1016/j.ajo.2012.05.007
Provis JM, Hendrickson AE (2008) The foveal avascular region of developing human retina. Arch Ophthalmol 126:507–511. https://doi.org/10.1001/archopht.126.4.507
Springer AD, Hendrickson AE (2005) Development of the primate area of high acuity, 3: temporal relationships between pit formation, retinal elongation and cone packing. Vis Neurosci 22:171–185. https://doi.org/10.1017/S095252380522206X
Mirhajianmoghadam H, Jnawali A, Musial G, Queener HM, Patel NB, Ostrin LA, Porter J (2020) In vivo assessment of foveal geometry and cone photoreceptor density and spacing in children. Sci Rep 10:8942. https://doi.org/10.1038/s41598-020-65645-2
Provis JM, Dubis AM, Maddess T, Carroll J (2013) Adaptation of the central retina for high acuity vision: cones, the fovea and the avascular zone. Prog Retin Eye Res 35:63–81. https://doi.org/10.1016/j.preteyeres.2013.01.005
Springer AD, Hendrickson AE (2004) Development of the primate area of high acuity. 1. Use of finite element analysis models to identify mechanical variables affecting pit formation. Vis Neurosci 21:53–62. https://doi.org/10.1017/s0952523804041057
Springer AD, Hendrickson AE (2004) Development of the primate area of high acuity. 2. Quantitative morphological changes associated with retinal and pars plana growth. Vis Neurosci 21:775–790. https://doi.org/10.1017/S0952523804215115
Liu X, Shen M, Yuan Y, Huang S, Zhu D, Ma Q, Ye X, Lu F (2015) Macular thickness profiles of intraretinal layers in myopia evaluated by ultrahigh-resolution optical coherence tomography. Am J Ophthalmol. https://doi.org/10.1016/j.ajo.2015.03.012
Jin P, Zou H, Zhu J, Xu X, Jin J, Chang TC, Lu L, Yuan H, Sun S, Yan B, He J, Wang M, He X (2016) Choroidal and retinal thickness in children with different refractive status measured by swept-source optical coherence tomography. Am J Ophthalmol 168:164–176. https://doi.org/10.1016/j.ajo.2016.05.008
Jonas JB, Xu L, Wei WB, Pan Z, Yang H, Holbach L, Panda-Jonas S, Wang YX (2016) Retinal thickness and axial length. Invest Ophthalmol Vis Sci 57:1791–1797. https://doi.org/10.1167/iovs.15-18529
Xiuyan Z, Qingmei T, Qiuxin W, Tailiang L, Jing X, Guodong T, Ting Y, Shasha L, Xi C, Chenying Q, Dongxue D, Jike S, Hongsheng B (2021) Thickness, vessel density of retina and choroid on OCTA in young adults (18–24 years old). Microvasc Res 136:104169. https://doi.org/10.1016/j.mvr.2021.104169
Del-Prado-Sanchez C, Seijas-Leal O, Gili-Manzanaro P, Ferreiro-Lopez J, Yanguela-Rodilla J, Arias-Puente A (2021) Choroidal, macular and ganglion cell layer thickness assessment in Caucasian children measured with spectral domain optical coherence tomography. Eur J Ophthalmol 31:3372–3378. https://doi.org/10.1177/1120672120965486
Zhang W, Shi T, Chen S, Chen H (2022) Subfoveal scleral thickness is associated with peripheral retinal changes in high myopia in children and adolescents. Int Ophthalmol. https://doi.org/10.1007/s10792-021-02153-w
Wagner-Schuman M, Dubis AM, Nordgren RN, Lei Y, Odell D, Chiao H, Weh E, Fischer W, Sulai Y, Dubra A, Carroll J (2011) Race- and sex-related differences in retinal thickness and foveal pit morphology. Invest Ophthalmol Vis Sci 52:625–634. https://doi.org/10.1167/iovs.10-5886
Read SA, Alonso-Caneiro D, Vincent SJ (2017) Longitudinal changes in macular retinal layer thickness in pediatric populations: myopic vs non-myopic eyes. PLoS ONE 12:e0180462. https://doi.org/10.1371/journal.pone.0180462
Healey N, McLoone E, Mahon G, Jackson AJ, Saunders KJ, McClelland JF (2013) Investigating the relationship between foveal morphology and refractive error in a population with infantile nystagmus syndrome. Invest Ophthalmol Vis Sci 54:2934–2939. https://doi.org/10.1167/iovs.12-11537
Thomas MG, Kumar A, Mohammad S, Proudlock FA, Engle EC, Andrews C, Chan WM, Thomas S, Gottlob I (2011) Structural grading of foveal hypoplasia using spectral-domain optical coherence tomography a predictor of visual acuity? Ophthalmology 118:1653–1660. https://doi.org/10.1016/j.ophtha.2011.01.028
Marmor MF, Choi SS, Zawadzki RJ, Werner JS (2008) Visual insignificance of the foveal pit: reassessment of foveal hypoplasia as fovea plana. Arch Ophthalmol 126:907–913. https://doi.org/10.1001/archopht.126.7.907
Chui TY, Zhong Z, Song H, Burns SA (2012) Foveal avascular zone and its relationship to foveal pit shape. Optom Vis Sci 89:602–610. https://doi.org/10.1097/OPX.0b013e3182504227
Doguizi S, Yilmazoglu M, Kiziltoprak H, Sekeroglu MA, Yilmazbas P (2019) Quantitative analysis of retinal microcirculation in children with hyperopic anisometropic amblyopia: an optical coherence tomography angiography study. J AAPOS. https://doi.org/10.1016/j.jaapos.2019.01.017
Bayraktar Z, Pehlivanoglu S, Bayraktar S, Albayrak S, Karakaya M (2020) Inter-ocular symmetry of vascular density and retinal thickness in unilateral anisometropic amblyopia. Clin Ophthalmol 14:1261–1267. https://doi.org/10.2147/OPTH.S234294
Kiziltoprak H, Tekin K, Cevik S, Kocer AM, Goker YS (2020) Normative data assessment of peripapillary and macular vessel density and foveal avascular zone metrics using optical coherence tomography angiography in children. J Pediatr Ophthalmol Strabismus 57:388–398. https://doi.org/10.3928/01913913-20200903-01
Sampson DM, Gong P, An D, Menghini M, Hansen A, Mackey DA, Sampson DD, Chen FK (2017) Axial length variation impacts on superficial retinal vessel density and foveal avascular zone area measurements using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 58:3065–3072. https://doi.org/10.1167/iovs.17-21551
Zhang Y, Zhang B, Fan M, Gao X, Wen X, Li Z, Zeng P, Tan W, Lan Y (2020) The vascular densities of the macula and optic disc in normal eyes from children by optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 258:437–444. https://doi.org/10.1007/s00417-019-04466-0
Acknowledgements
We would like to thank Proofed for English editing.
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
ASS, SO, SAB, İA, GY and MYÇ all contributed to the conception and design of the work; the acquisition, analysis, and interpretation of data; and drafting and revising the manuscript critically for important intellectual content; and final approval of the version to be published; and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Başkent University (Date: 07.09.2021 / No: KA21/376).
Consent to participate
Written informed consent was obtained from the participants’ legal guardians to participate in the study.
Consent to publish
The authors affirm that consent to publish participants’ data has been received from all participants’ legal guardians.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sarıgül Sezenöz, A., Oto, S., Akça Bayar, S. et al. A variation of foveal morphology in a group of children with hypermetropia. Int Ophthalmol 43, 2947–2956 (2023). https://doi.org/10.1007/s10792-023-02701-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10792-023-02701-6