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Development of Refractive Errors-What Can We Learn View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Erasmus University Digital Repository Development of Refractive Errors—What Can We Learn From Inherited Retinal Dystrophies? MICHELLE HENDRIKS, VIRGINIE J.M. VERHOEVEN, GABRIE¨LLE H.S. BUITENDIJK, JAN ROELOF POLLING, MAGDA A. MEESTER-SMOOR, ALBERT HOFMAN, RD5000 CONSORTIUM, MAARTEN KAMERMANS, L. INGEBORGH VAN DEN BORN, AND CAROLINE C.W. KLAVER PURPOSE: It is unknown which retinal cells are degree of myopia and in CABP4 (SE 4.81 D [SD 0.35]) involved in the retina-to-sclera signaling cascade causing with the highest degree of hyperopia. myopia. As inherited retinal dystrophies (IRD) are char- CONCLUSIONS: Refractive errors, in particular acterized by dysfunction of a single retinal cell type and myopia, are common in IRD. The bipolar synapse and have a high risk of refractive errors, a study investigating the inner and outer segments of the photoreceptor may the affected cell type, causal gene, and refractive error in serve as critical sites for myopia development. (Am J IRDs may provide insight herein. Ophthalmol 2017;182:81–89. Ó 2017 Elsevier Inc. All DESIGN: Case-control study. rights reserved.) METHODS: STUDY POPULATION: Total of 302 patients with IRD from 2 ophthalmogenetic centers in the Netherlands. REFERENCE POPULATION: Population-based EFRACTIVE ERRORS (MYOPIA AND HYPEROPIA) ARE Rotterdam Study-III and Erasmus Rucphen Family Study the most common ocular disorders worldwide and 1 (N [ 5550). Distributions and mean spherical equiva- R are a prominent cause of blindness. This highly lent (SE) were calculated for main affected cell type and heritable trait has been subject to many studies, and the causal gene; and risks of myopia and hyperopia were eval- search for genes—in particular for myopia—has been 2,3 uated using logistic regression. ongoing for several years. Myopia is thought to be RESULTS: Bipolar cell-related dystrophies were associ- caused by a visually evoked retina-to-sclera-signaling ated with the highest risk of SE high myopia 239.7; cascade. Various genes representing different pathways in 4,5 odds ratio (OR) mild hyperopia 263.2, both P < myopia development have been discovered. These .0001; SE L6.86 diopters (D) (standard deviation [SD] pathways include neurotransmission, retinoic acid 6.38), followed by cone-dominated dystrophies (OR metabolism, extracellular matrix remodeling, and eye high myopia 19.5, P < .0001; OR high hyperopia development. Still, only a small proportion of the 5 10.7, P [ .033; SE L3.10 D [SD 4.49]); rod dominated heritability of refractive error has been uncovered. dystrophies (OR high myopia 10.1, P < .0001; OR high It is known that refractive errors are common in patients hyperopia 9.7, P [ .001; SE L2.27 D [SD 4.65]), and with inherited retinal dystrophies (IRD), such as retinitis 6 retinal pigment epithelium (RPE)-related dystrophies pigmentosa (RP, in particular in X-linked forms ), congen- (OR low myopia 2.7; P [ .001; OR high hyperopia ital stationary night blindness, Stargardt disease, and Best 7–9 5.8; P [ .025; SE L0.10 D [SD 3.09]). Mutations in macular dystrophy. IRDs are clinically and genetically RPGR (SE L7.63 D [SD 3.31]) and CACNA1F heterogeneous, usually causing degeneration of a primary (SE L5.33 D [SD 3.10]) coincided with the highest cell type, such as the retinal pigment epithelium (RPE), photoreceptors (cones and rods), or other retinal 10 Accepted for publication Jul 10, 2017. neurons. According to the location of retinal cell dysfunc- From The Rotterdam Eye Hospital, Rotterdam, Netherlands (M.H., tion, they can be classified into RPE-related macular dystro- L.I.B.); Departments of Ophthalmology (V.J.M.V., G.H.S.B., J.R.P., phies, photoreceptor dystrophies (cone- and rod-dominated M.A.M.-S., C.C.W.K.), Epidemiology (V.J.M.V., G.H.S.B., M.A.M.-S., A.H., C.C.W.K.), and Clinical Genetics (V.J.M.V.), Erasmus Medical dystrophies), and inner retina dystrophies (bipolar cell dys- Center, Rotterdam, Netherlands; Netherlands Consortium for Healthy functions). Stargardt disease, caused by mutations in the Ageing, Netherlands Genomics Initiative, The Hague, Netherlands ABCA4 gene, is the most common form of macular dystro- (A.H.); Department of Epidemiology, Harvard T.H. Chan School of 11,12 Public Health, Boston, Massachusetts (A.H.); Netherlands Institute for phy. Other more rare RPE-related macular dystrophies Neuroscience, Amsterdam, Netherlands (M.K.); Department of are Best macular dystrophy and pattern dystrophy. Cone- Neurogenetics, Academic Medical Center, University of Amsterdam, dominated dystrophies include achromatopsia, cone dystro- Amsterdam, Netherlands (M.K.); and Department of Ophthalmology, 13 Radboud University Medical Center, Nijmegen, Netherlands phies (CD), and cone-rod dystrophies (CRD). Rod-cone (C.C.W.K.). dystrophies (RCD), also known as RP, are the largest sub- ÃA listing of the members of the RD5000 Consortium is included in the type of IRD, accounting for w50% of all inherited Appendix. IRDs.14 Lastly, congenital stationary night blindness Inquiries to Caroline C. W. Klaver, Erasmus Medical Center, Room Na- 2808, PO Box 2040, 3000 CA, Rotterdam, The Netherlands; e-mail: c.c.w. (CSNB) is usually caused by defective retinal signaling 15 [email protected] from the photoreceptors to the ‘‘ON’’ bipolar cells. 0002-9394/$36.00 © 2017 ELSEVIER INC.ALL RIGHTS RESERVED. 81 http://dx.doi.org/10.1016/j.ajo.2017.07.008 IRDs may serve as naturally occurring experiments to For RS-III and ERF (reference group) a similar protocol study the specific cell types and structures involved in the was used for phenotyping; all subjects underwent an development of myopia. Although several former reports ophthalmologic examination, which included noncyclo- refer to an increased incidence of myopia in patients with plegic automated measurement of refractive error (Topcon inherited retinal dystrophies, most do not include specific RM-A2000 autorefractor, Tokyo, Japan), followed by sub- quantifiable data, and their spectrum of diseases is jective refraction, best-corrected visual acuity, fundus limited.6,7,16 photography, and visual field perimetry (Humphrey Visual Here, we studied a large group of patients with a broad Field Analyzer; Zeiss, Oberkochen, Germany). spectrum of inherited IRDs. We investigated frequency and degree of refractive error as a function of affected cell MOLECULAR GENETIC ANALYSIS: In the outpatient type and causal gene, with the aim to detect bottlenecks clinic, patients with inherited IRDs were offered DNA for myopia development. analysis for diagnostic testing. DNA was isolated from pe- ripheral blood lymphocytes using standard procedures. ABCA4 gene mutations were analyzed in CD and RD pa- tients with microarray screening from Asper Biotech METHODS (Tartu, Estonia). Genotyping was performed using the autosomal recessive and autosomal dominant RP chip SUBJECTS: IRD patients were identified at ophthalmoge- from Asper Biotech (Tartu, Estonia). In patients with RP netic outpatient clinics of Erasmus Medical Center (n ¼ and deafness suspected for Usher syndrome an additional 265) and the Rotterdam Eye Hospital (n ¼ 37). These 2 USH chip from Asper Biotech was used. All mutations ophthalmogenetic centers belong to the Dutch IRD regis- were confirmed with Sanger sequencing. When one muta- try, the RD5000 Consortium.17 The total study population tion was found with the autosomal recessive or Usher chip, consisted of 302 patients with IRD, and we identified 4 the whole gene was sequenced in order to identify a second groups of primary affected cell type: RPE-related macular mutation, if present. X-linked CRD or X-linked RCD dystrophies (RPE; Stargardt and Best disease and PD; n ¼ probands were screened for mutations in the RPGR gene. 77), cone-dominated dystrophies (CD; achromatopsia, Patients clinically diagnosed with CSNB were screened CRD, n ¼ 76), rod-dominated dystrophies (RD; RP and for mutations in the CACNA1F, TRPM1, CABP4, and RCD; n ¼ 104), and ON bipolar cell dysfunctions NYX gene. (BPCD; n ¼ 45). To compare the distribution of refractive error to a general population, we used a population-based STATISTICAL ANALYSIS: Spherical equivalent (SE) was reference group (n ¼ 5550), a combined dataset from calculated according to the standard formula (SE ¼ 2940 participants (age 45þ years) from the Rotterdam sphere þ ½ cylinder), and the mean of both eyes was Study III (RS-III),18 and 2610 participants (age 18þ years) used for analysis. When data from only 1 eye were avail- from the Erasmus Rucphen Family Study (ERF).19,20 able, the SE of this eye was used. We categorized SE into Data of IRD patients enrolled in the RD5000 database low (SE from À1.5 to À3 diopters [D]), moderate were pseudonymized and personal details were only avail- (SE from À3toÀ6 D), and high (SE of À6 D or lower) able at their ophthalmological center, which makes myopia; emmetropia (SE from À1.5 to þ1.5 D); and informed consent not obligatory. Nevertheless, we created low (SE from þ1.5 to þ3 D), moderate (SE from þ3 an informed consent to obtain patient approval for data en- to þ6 D), and high (SE of þ6 D or higher) hyperopia, using try in the RD5000 database. Measurements in the Rotter- previously defined criteria.22 dam Study and ERF were collected after receiving Analyses were stratified by main affected cell type (RPE, approval from the Medical Ethics Committee of the Eras- CD, RD, or BPCD) and by causal gene. Causal genes that mus University Medical Center, and all participants pro- were found in fewer than 3 patients were pooled into a sin- vided written informed consent in accordance with the gle group (‘‘other genes’’). Logistic regression analyses were Declaration of Helsinki. used to assess the risk of low, moderate, and high myopia and hyperopia vs emmetropia per disease group, using the CLINICAL ASSESSMENT: We retrieved all clinical data RS-III and ERF study as the reference group, and adjusting from medical charts.
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