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Bjophthalmol-2020-316528 1..7 Clinical science Br J Ophthalmol: first published as 10.1136/bjophthalmol-2020-316528 on 24 June 2020. Downloaded from Reduced vessel density in deep capillary plexus correlates with retinal layer thickness in choroideremia Alessandro Arrigo ,1 Francesco Romano ,1,2 Maurizio Battaglia Parodi,1 Peter Charbel Issa,3,4 Johannes Birtel,3,4,5 Francesco Bandello ,1 Robert E Maclaren6 1Department of Ophthalmology, ABSTRACT degrees of photoreceptor and RPE degeneration – Scientific Institute San Raffaele, Background To assess retinal layer thickness in in affected areas.6 10 A loss of nuclei has been University Vita-Salute, via choroideremia (CHM) and to reveal its correlation with observed in the inner retina in postmortem Olgettina, 60, 20132, Milan, 8 Italy optical coherence tomography (OCT) angiography (OCTA) tissue. 2Eye Clinic, Department of findings. Patients with CHM generally report nyctalopia in Biomedical and Clinical Science, Methods The study was designed as an observational, the first two decades of life, and the disease may lead Luigi Sacco University Hospital, cross-sectional clinical series of patients with CHM, which to blindness in middle age.34However, since visual Milano, Italy ’ 3Oxford Eye Hospital, Oxford included 14 CHM eyes and 14 age-matched controls. acuity does not deteriorate until the disease s late University Hospitals NHS Multimodal imaging included OCT and OCTA. The vessel stages, anatomical endpoints may provide addi- Foundation Trust, Oxford, UK density (VD) of superficial capillary (SCP), deep capillary tional help in determining disease progression. 4 Nuffield Laboratory of (DCP) and choriocapillaris (CC) plexuses was analysed by Numerous ophthalmic imaging studies have studied Ophthalmology, Nuffield OCTA. The apparently preserved retinal islet and atrophic morphological and functional alterations in Department of Clinical 11–19 Neurosciences, University of regions were investigated separately. Main outcome CHM. However, no study has thoroughly Oxford, Oxford, UK measures were as follows: best-corrected visual acuity investigated quantitative alterations occurring in 5Department of Ophthalmology, (BCVA), total retinal layers, ganglion cell layer (GCL), retinal layers. University of Bonn, Bonn, inner plexiform layer (IPL), inner nuclear layer (INL), outer The goal of this study was to assess retinal layer Germany 6Oxford Eye Hospital, Oxford plexiform layer (OPL), outer nuclear layer (ONL), ellipsoid thickness in patients with CHM by performing mea- University Hospitals NHS zone–retinal pigment epithelium (EZ-RPE) layer, choroidal surements both in the apparently preserved central Foundation Trust, and Nuffield thickness and VDs of SCP, DCP and of CC. islet and in the atrophic retina, and to correlate Laboratory of Ophthalmology, Results Mean BCVA was 0.0±0.0 LogMAR in both these findings with optical coherence tomography Nuffield Department of Clinical fi (OCT) angiography (OCTA) data. Neurosciences, University of groups. GCL, ONL, EZ-RPE and choroid were signi cantly Oxford, Oxford, UK thinned in CHM, particularly in the atrophic region. OPL was unaffected in the apparently preserved islet, whereas MATERIALS AND METHODS Correspondence to INL and IPL were similarly thinned in the atrophic and The study was designed as an observational, cross- Alessandro Arrigo, Department apparently preserved retina. DCP appeared severely sectional clinical series of patients with CHM. of Ophthalmology, IRCCS affected in both regions, while CC was only altered in the Ospedale San Raffaele, Patients and healthy controls were consecutively atrophic retina. Significant correlations were found University Vita- Salute, Via recruited from the Inherited Retinal Dystrophy http://bjo.bmj.com/ between OCT and OCTA parameters. Olgettina 60, Milan 20132, Units at the Department of Ophthalmology, Italy; alessandro. arrigo@ Conclusions Our study showed severe alterations in Scientific Institute San Raffaele, Milan, Italy, and hotmail. com both outer and inner retinal layers of patients with CHM. the Department of Ophthalmology, University of The extended retinal involvement might be the Received 8 April 2020 Bonn, Germany. Written informed consent was consequence of neuronal and vascular trophic factor Revised 19 May 2020 obtained from all subjects, and the study adhered Accepted 29 May 2020 reduction produced by the primarily altered RPE and/or Published Online First to the tenets of the Declaration of Helsinki. The secondary Müller glial cell reaction. on September 27, 2021 by guest. Protected copyright. 24 June 2020 study was approved by the Ethical Committee of Scientific Institute San Raffaele, Milan (NET-2016- 02363765). Inclusion criteria included (1) a genetically con- INTRODUCTION firmed clinical diagnosis of CHM, (2) foveal sparing Choroideremia (CHM) is an X-linked recessive and (3) clear optical media. Exclusion criteria retinal disease characterised by gradual and cen- included (1) the presence of other retinal or optic tripetal chorioretinal degeneration, with the fun- nerve disorders, (2) cystoid macular oedema, (3) dus having a typically pale end-stage refractive errors greater than ±3 D, (4) previous – appearance.1 4 The disease is caused by mutations ophthalmic surgery and systemic conditions poten- in the CHM gene that encodes the Rab escort tially altering retinal anatomy and function. The © Author(s) (or their protein-1, which interacts with Rab27a, an intra- control group did not reveal any ocular or systemic employer(s)) 2021. Re- use cellular protein involved in protein prenylation diseases, and was age-matched, sex-matched and permitted under CC BY- NC. No commercial re- use. See rights and is believed to be necessary for vesicle traffick- ethnicity-matched with the patient group. 5 and permissions. Published ing in the retinal pigment epithelium (RPE). Both cohorts underwent a complete ophthalmo- by BMJ. Several histological reports carry images depicting logic examination, including best-corrected visual To cite: Arrigo A, Romano F, the chorioretinal degeneration, including an inde- acuity (BCVA) testing, slit-lamp biomicroscopy, Parodi MB, et al. pendent choriocapillaris (CC), RPE and outer Goldmann applanation tonometry, funduscopic Br J Ophthalmol retina degeneration; areas of well-preserved retina examination, colour fundus photography (TRC- 2021;105:687–693. in the vicinity of severe atrophy; and discordant 50DX, Topcon Corporation; Tokyo, Japan, or Arrigo A, et al. Br J Ophthalmol 2021;105:687–693. doi:10.1136/bjophthalmol-2020-316528 687 Clinical science Br J Ophthalmol: first published as 10.1136/bjophthalmol-2020-316528 on 24 June 2020. Downloaded from Visucam, Zeiss, Oberkochen, Germany), blue-light fundus auto- Differences in thickness were studied by means of analysis of fluorescence (BL-FAF) and spectral domain-OCT (SD-OCT; variance for repeated measures and Bonferroni’s correction for Spectralis HRA+OCT, Heidelberg Engineering; Heidelberg, posthoc analysis. The relationship between morphological and Germany). A subgroup underwent 12×12-mm OCTA examina- epidemiological variables was explored using Kendall’s Tau-b tion (DRI TritonOCT, TopconCorporation; or PLEX Elite 9000, (non-parametric) correlation test. Results for descriptive analyses ZEISS, Dublin, California, USA). The acquisition protocol are expressed as mean±SD for quantitative values and as fre- included a single-line SD-OCT acquisition (1024 A-scans per B- quency and percentages for categorical ones. Interobserver line scan; automatic real time (ART)=100 frames), passing reproducibility for the measurement of all the different layers through the fovea. Eye tracking was enabled during the examina- was evaluated by means of intraclass correlation coefficients tion. Two independent graders (FR and AA) measured retinal (95% CIs). Statistical significance was set at p<0.05, with all layers. In patients with CHM, measurements were performed at the analyses being performed using the SPSS Statistics Version the point of maximal foveal thickness in the apparently preserved 21.0 Software package (IBM; Armonk, New York, USA). retina, within a 1.5 mm diameter area centred on the middle of the fovea, and 100 μm external to the boundary between the RESULTS apparently preserved retina and the atrophic retina. In the con- Overall, 14 patients with CHM (14 eyes) and 14 healthy male trols, the thickest foveal site was evaluated. The following were controls were included. Mean age was 38.2±8.9 years (range: assessed: total retinal layer, ganglion cell layer (GCL), inner plexi- 23–56; median: 36) and 35.3±8.2 (range: 27–51; median: 36) form layer (IPL), inner nuclear layer (INL), outer plexiform layer for patients and controls, respectively. LogMAR BCVA was 0.0 (OPL), outer nuclear layer (ONL) and ellipsoid zone–RPE(EZ- ±0.0 for both groups. No differences in age, ethnicity or intrao- RPE) layer.20 The mean of the two independent measurements cular pressure were observed (all p>0.05). A specimen case of from the same structural scan was used for the statistical analysis. CHM is shown in figure 1. The areas of apparently preserved retina were outlined on the BL- Statistical analysis revealed significant retinal and choroidal FAF image. On OCTA, vessel densities (VDs) from the superficial thinning in patients with CHM compared with controls capillary (SCP), deep capillary (DCP) and CC) plexuses were (F=160.8 and 135.6, respectively; both p<0.001). Quantitative independently quantified in the apparently preserved and in the measurement of total
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