Decreased choroidal thickness in vitiligo patients

Decreased choroidal thickness in vitiligo patients Background: Vitiligo is a disease characterized by depigmented macules and patches that occur as a result of the loss of functional melanocytes from the affected skin through a mechanism which has not been elucidated yet. Destruction of pigment cells in vitiligo may not remain limited to the skin; the eyelashes, iris, ciliary body, choroid, retinal pigment epithelium and meninges may also be affected. This study aims to compare the choroidal thickness of patients with and without vitiligo using optical coherence tomography (OCT). Methods: Spectral-domain optical coherence tomography (SD-OCT) (Retina Scan Advanced RS-3000 NIDEK, Japan) instrument (with λ = 840 nm, 27,000 A-scans/second and 5 μm axial resolution) was used for the imaging. Statistical analysis was performed using SPSS 21.0 software package. Results: In all values except optic nevre area measurements, the choroidal thickness of all vitiligo patients was found out to be thinner compared to the control group. Conclusions: In vitiligo, the choroidal thickness may be affected by the loss of melanocytes. Keywords: Vitiligo, Choroidal thickness, OCT, VASI, Oculocutaneous disease Background large-caliber vessels (known as Sattler’sand Haller’s Vitiligo is a disease characterized by depigmented layers, respectively), and a suprachoroidal layer, all macules and patches that occur as a result of the loss embedded within a collagenous and elastic stroma of functional melanocytes from the affected skin along with melanocytes [5]. The choroidal changes in through a mechanism which has not been elucidated many ocular pathological conditions such as polypoi- yet. The frequency of vitiligo throughout the world dal choroidal vasculopathy and age related macular changes in the rate of 0.5–2% and does not vary degeneration were reported [6]. Choroidal thickness depending on gender and race [1–3]. While vitiligo changes has also previously been observed in many may occur at all ages soon after birth, the average systemic inflammatory disorders [6–9]. age of onset is approximately 20 years [1–3]. Melanocytes in the eyes consist of neural crest cells The choroid is a vascularized and pigmented tissue that have migrated ventrally. These melanocytes are which was first examined histologically in the 17th located in the uveal tract (choroid, ciliary body, and century and then tried to be visualized by various the iris). Especially the stroma of the choroid layer methods [4]. The choroid of the eye is a highly consists of a high number of melanocytes [5]. The vascularized structure that supplies the outer retina melanin, which is produced in melanocytes in the and, histologically, consists of a thin choriocapillaris choroid layer, has an important function in an area layer that is adjacent to the retinal pigment epithe- starting from the retina and extending to the visual lium (RPE) and Bruch’s membrane, medium- and cortex of the brain. Melanin, which is produced in melanocytes in the eye and stored in melanosomes, * Correspondence: serkan.demirkan@yahoo.com.tr has a very important role in the protection of the eye Department of Dermatology and Venerology, Kirikkale University Faculty of from the intraocular reflections of the light [5]. Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, Turkey Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 2 of 6 Destruction of pigment cells in vitiligo may not remain diabetes, cigarette use, hypertension, antihypertensive limited to the skin; the eyelashes, iris, ciliary body, chor- drug use, known atherosclerotic disease, pregnancy, oid, retinal pigment epithelium and meninges may also macular degenerations, previous ocular surgery, choroidal be affected [10]. Low choroidal thickness may be ex- pathology, glaucoma, high refractive error (patients with pected in vitiligo where melanocyte loss proceeds [10]. more than + 6 and −6 diopters as cycloplegic spherical Although there have been many studies conducted to equivalent), best corrected visual acuity below 20/25, and evaluate choroidal thickening in diseases that affected patients with a systemic other disease were not in- eye vasculature, limited research has been conducted on cluded in this study. Spectral-domain optical coher- the diseases that affect melanocytes and another compo- ence tomography (SD-OCT) (Retina Scan Advanced nent of choroidal tissue, which remained under-researched. RS-3000 NIDEK, Japan) instrument (with λ = 840 nm, This study aims to compare the choroidal thickness of 27,000 A-scans/second and 5 μm axial resolution) patients with and without vitiligo using optical coher- was used for the imaging. ence tomography (OCT). Before evaluation, using EDI-OCT scanning, the cen- tral macular thickness was measured in the right eye of Methods each patient. Choroidal and scleral boundaries were This prospective clinical study addresses the examin- drawn with the assistance of software programs. Chor- ation of the bilateral eyes of (154 eyes). A total of 77 in- oidal thickness was measured at the center of the fovea dividuals, including 34 vitiligo and 43 non-vitiligo, were (SubF), and 500 μm nasally, temporally, superiorly and included in the study. This study was carried out be- inferiorly (N1, T1, S1, I1), and 1500 μm (N2, T2, S2, I2) tween 2015 and 2016 in accordance with the tenets of from the center of the fovea. The peripapillary region the Declaration of Helsinki. The study protocol was ap- was measured 500 μm (N, T, S, I) from the center of proved by the Local Ethical Committee of the University the optic nerve. The averages of upper hemifield, lower of Kırıkkale. All patients and control subjects voluntarily hemifield, and whole hemifield of the peripapillary re- participated in this study and signed an informed con- gion were also measured (Fig. 1a, b). The foveal and sent form. parafoveal choroidal thickness was determined by Patients, who were diagnosed with vitiligo and were measuring the region between the outer border of the aged between 20 and 50 years, and non-vitiligo adults retinal pigment epithelium layer and the sclero-choroidal with similar characteristics participated in this study. interface manually. Measurements in the peripapillary VASI (vitiligo area severity index), which shows the de- area were carried out automatically with the instrument. pigmentation extent, was calculated in all vitiligo pa- The values of the right and left eyes of the patient and tients [11]. The percentage of the body area involved can control group were separately specified and compared. All be estimated by the so-called 1% rule or “palm method”. measurements are presented with median, minimum and In both children and adults, the palm of the hand, in- maximum values. cluding the fingers, is approximately 1% of the total body Statistical analysis was performed using SPSS 21.0 soft- surface area (TBSA), and it describes hand unit [11]. For ware package. Descriptive statistics were presented as a each body region, the VASI was determined by the prod- mean ± standard deviation. In comparisons between pa- uct of the area of vitiligo in hand units and the extent of tient and control groups, the student’s t-test was applied depigmentation within each hand unit–measured patch to numerical data that followed a normal distribution, (possible values of 0, 10, 25, 50, 75, 90% or 100%). The while the Mann-Whitney U test was applied to data total body VASI was calculated using the following for- that did not follow a normal distribution. The Pearson mula considering the contributions of all body regions correlation test was applied to normally distributed (possible range, 0–100): measurements, and the Spearman correlation test was applied to data that did not follow a normal distribu- VASI ¼ All Body Sites½ Hand Units tion. The statistical significance value was accepted as p <0.05. ½ Residual Depigmentation All participants had a thorough ophthalmologic exam- Results ination, uncorrected visual acuity, best corrected visual Thirty four vitiligo patients and 43 individuals without acuity, manifest refraction, cycloplegic refraction and vitiligo diagnosis were included in the study. The mean slit-lamp examination. Intraocular pressures were mea- age of the vitiligo patients was 39.2 years, and the aver- sured with an air-puff tonometer. Dilated fundus exami- age age of the individuals in the control group was nations were performed using a 78 D lens. 39.3 years. Table 1 shows the age and sex distrubation, Individuals with poor OCT quality having a history intraocular pressure, axial length, visual acuity, and re- that may have affected the choroidal thickness, such as fraction defect values of the patients and control group. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 3 of 6 Fig. 1 a, b The areas of choroidal thickness measurements In all values except optic nerve area measurements, Discussion the choroidal thickness of all vitiligo patients was found The stroma of the choroid layer consists of a high num- out to be thinner compared to the control group ber of melanocytes [5]. Destruction of pigment cells in (Table 2). Correlation between VASI values of vitiligo vitiligo may not remain limited to the skin; the eye- patients and age, duration of disease, and choroidal lashes, iris, ciliary body, choroid, retinal pigment epithe- thickness were signed in Table 3. lium and meninges may also be affected [10]. A low There was a negative correlation between age and choroidal thickness may be expected in vitiligo where choroidal thickness in some areas in patients. In pa- melanocyte loss proceeds [10]. To our knowledge, this is tients and control groups, gender had an effect on the first study that examined the relation between chor- the choroidal difference in none of the measured oidal changes and vitiligo in adulthood. regions (p > 0.05). There was no correlation between The choroid covers the outer retina and is among the duration of disease and choroidal thickness in all most vascularized tissues in the body. This tissue sup- areas. plies oxygen and nutrition to and provides temperature In those with higher VASI value, periorbital involve- regulation for the retina. Also, choroid-containing me- ment was significantly more frequent. (p = 0.029). lanocytes prevent intraocular reflections. In the eye, The frequency of periorbital involvement increased choroidal thickness may be affected by several factors, with the duration of the disease (p < 0.001). The peri- such as age, axial length, and refractive errors [12, 13]. orbital involvement did not have an effect on chor- A number of studies have found that choroidal thick- oidal thickness in patients with vitiligo. There was no ness plays a prognostic or predictive role in various statistically significant difference between those with local (e.g., diabetic retinopathy), and systemic diseases and without periorbital involvement concerning age (e.g., hypertension, anemia, rheumatoid arthritis and (p = 0.300). obesity) [14–20]. Table 1 Age and sex distrubation, intraocular pressure, axial length, visual acuity, refraction defect values of the patients and control group Patients (n:34) Control group (n:43) P value (mean±) (mean±) Age 39.2 ± 16.14 39.3 ± 12.51 0.101* Sex(F/M) 15:19 (44%:56%) 20:23 (46%:54%) Right intraocular pressures 14.20 ± 3.31 15.00 ± 2.23 0.105* Left intraocular pressures 14.55 ± 2.83 14.76 ± 2.09 0.347* Axial length 23.57 ± 1.04 23.58 ± 1.22 0.960* Right eyes visual acuity 0.07 ± 0.21 −0.01 ± 0.26 0.330* Left eyes visual acuity 0.08 ± 0.22 0.06 ± 0.40 0.845* Right eye refraction defect − 0.37 ± 1.00 0.00 ± 0.92 0.184* Left eyes refraction defect −0.21 ± 0.97 − 0.01 ± 0.98 0.702* *…Student’s t test Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 4 of 6 Table 2 Mean choroidal thickness in vitiligo patients and control group individuals Patient (n:34) Control (n:43) P value Mean ± SD Minimum Median Maximum Mean ± SD Minimum Median Maximum Right, SubF 220.2 ± 39.8 170 224 290 261.4 ± 31.1 168 256 305 < 0.001** Right, N1 223.6 ± 42.1 163 220 276 258.4 ± 32.5 190 248 302 < 0.001** Right, N2 226.0 ± 39.2 130 220 340 261.5 ± 37.4 200 265 361 < 0.001* Right, T1 220.5 ± 39.9 143 224 303 257.9 ± 34.2 139 257.5 311 < 0.001** Right, T2 225.2 ± 41.1 109 220 280 253.4 ± 32.3 200 250 327 0.001* Right, S1 222.9 ± 44.6 142 219 296 268.7 ± 38.1 198 271 289 < 0.001** Right, S2 217.8 ± 40.8 151 219 301 259.1 ± 33.4 201 261 306 < 0.001** Right, I1 223.4 ± 45.2 119 221 289 266.3 ± 37.0 136 264 321 < 0.001** Right, I2 224.5 ± 45.2 117 226 340 265.9 ± 34.9 200 260 360 < 0.001* Right optic nerve, LowH 95.0 ± 15.4 34 96 138 97.5 ± 7.9 80 97 118 0.429* Right optic nerve, UpH 80.2 ± 16.8 43 81 128 77.1 ± 16.8 41 79 135 0.418** Right optic nerve, WholP 98.9 ± 15.2 47 97 134 100.5 ± 8.1 54 101 126 0.805* Right optic nerve, N 80.2 ± 16.8 54 77.5 126 77.1 ± 16.8 33 75 117 0.418** Right optic nerve, T 68.9 ± 14.1 45 68 104 68.4 ± 15.5 29 69 99 0.689* Right optic nerve, S 128.9 ± 25.3 59 132 168 129.4 ± 16.5 95 129 175 0.712* Right optic nerve, I 118.9 ± 23.6 21 125.5 175 125.6 ± 17.0 79 125 165 0.230* Left, SubF 222.7 ± 37.3 118 223 296 269.1 ± 31.0 129 267 305 < 0.001** Left, N1 223.7 ± 38.5 105 224 301 271.7 ± 36.1 119 269 301 < 0.001** Left, N2 228.2 ± 39.6 106 227 298 265.4 ± 35.8 129 267 311 < 0.001** Left, T1 227.2 ± 42.2 164 226.5 380 308.2 ± 30.8 210 265 291 < 0.001* Left, T2 235.4 ± 38.3 131 234 324 272.7 ± 35.7 176 275 329 < 0.001** Left, S1 215.3 ± 40.2 126 216 305 257.2 ± 35.2 161 254 298 < 0.001** Left, S2 220.0 ± 37.6 137 219 299 249.5 ± 48.2 148 251 324 0.005** Left, I1 216.5 ± 38.0 139 218 301 262.3 ± 31.7 167 264 341 < 0.001** Left, I2 222.2 ± 37.1 170 220 344 262.8 ± 31.9 210 260 350 < 0.001* Left optic nerve, LowH 94.8 ± 12.2 59 95 141 95.5 ± 11.0 48 97 173 0.955* Left optic nerve, UpH 122.6 ± 19.5 75 96 124 127.3 ± 16.3 77 93 125 0.255** Left optic nerve, WholP 98.1 ± 12.0 70 99 125 100.2 ± 11.7 79 101 133 0.655* Left optic nerve, N 75.6 ± 21.6 30 78 126 82.1 ± 23.7 27 78 174 0.432* Left optic nerve, T 66.0 ± 18.1 35 61.5 106 65.0 ± 14.3 38 66 95 0.782* Left optic nerve, S 128.4 ± 19.9 81 131.5 162 128.6 ± 20.5 76 131 178 0.951* Left optic nerve, I 122.6 ± 19.5 89 122 169 127.3 ± 16.3 97 127 174 0.310* *…Mann Whitney U test **…Student’s t test In oculocutaneous albinism patients with melano- Vogt-Koyanagi-Harada Diseaseis a bilateral granu- cyte absence, the choroidal thickness in the subfoveal lomatous panuveitis associated with autoimmunity de- area was found to be significantly lower compared to veloped against melanocytes [22]. Patients with VKH the control group. However, no difference was found increased choroidal thickness, which is probably due to in the peripapillary region compared to the control exudation with inflammatory processes [23]. Invitiligo group [21]. Choroidal thickness measurement was patients, the inflammatory process is chronic and exuda- compared in a much higher number of regions in our tive is not observed. Therefore, despite the presence of study compared to the aforementioned study in which melanocyte destruction as it is in VKH, the increase in the lower choroidal thickness is also expected in choroidal thickness of vitiligo patients is not expected. vitiligo, which is another disease that proceeds with The study conducted by Bulbul-Baskan et al. showed melanocyte loss [21]. that eye pathology was observed in 10 of the 45 vitiligo Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 5 of 6 Table 3 Correlation between VASI values of vitiligo patients and Conclusion age, duration of disease, and choroidal thickness Melanin, which is produced in melanocytes in the eye VASI r p and stored in melanosomes, has a very important role in the protection of the eye from the intraocular reflections Age Weak correlation 0.349 0.043 of light. In this study, in all values except optic nerve Duration of disease Moderate correlation 0.555 < 0.001 area measurements, the choroidal thickness of all vitiligo Right fovea, horizontal Negative correlation −0.417 0.014 patients was found out to be thinner compared to the Right nasal 500 Negative correlation − 0561 0.001 control group. Right nasal 1500 Negative correlation −0.381 0.026 The melanocyte amount in the choroidal layer in Left fovea, vertical Negative correlation −0.437 0.010 vitiligo should be studied in the future postmortem and in vivo studies. Left superior 500 Negative correlation −0.481 0.004 Left inferior 500 Negative correlation −0.484 0.004 Abbreviations CT: Choroidal thickness; EDI-OCT: Enhanced-depth imaging optical Left superior 1500 Negative correlation −0.356 0.039 coherence tomography; I: Choroidal thickness at 500 μm inferior to the Left inferior 1500 Negative correlation −0.380 0.027 fovea; I1: Choroidal thickness at 500 μm inferior to the fovea; I2: Choroidal thickness at 1500 μm inferior to the fovea; LowH: LowerHemifield; …Pearson correlation test N: Choroidal thickness at 500 μm nasal to the fovea; N1: Choroidal thickness Spearman correlation test at 500 μm nasal to the fovea; N2: Choroidal thickness at 1500 μm nasal to the fovea; OCT: Optical coherence tomography; RPE: Retinal pigment patients. Their findings revealed that iris involvement epithelium; S: Choroidal thickness at 500 μm superior to the fovea; in one patient, ring-like peripapillary atrophy around S1: Choroidal thickness at 500 μm superior to the fovea; S2: Choroidal the optic nerve in seven patients, hyperpigmented rim thickness at 1500 μm superior to the fovea; SD-OCT: Spectral-domain optical coherence tomography; SubF: Choroidal thickness at fovea; T: Choroidal in the left top segment of the retinal pigment epithe- thickness at 500 μm temporal to the fovea; T1: Choroidal thickness at lium in addition to peripapillary atrophy in one patient, 500 μm temporal to the fovea; T2: Choroidal thickness at 1500 μm temporal focal hypopigmented dots in the temporal retinal area to the fovea; UpH: Upper Hemifield; VASI: Vitiligo area severity index; VKH: Vogt-Koyanagi-Harada; WholP: Whole peripapillary in one patient, and diffuse hypopigmentation in onepa- tient were observed [24]. Another study carried out Availability of data and materials with black patients with vitiligo, thin and dot-like pig- The data sets used and/or analysed during the current study are available from the corresponding author on reasonable request. mentary disturbances were identified in four of the 17 patients [25]. Authors’ contributions In the current study, we observed a significant re- SD, GS, ÖGand AAK collected patients and control group for the study.ZO, duction in OCT in all areas except optic nerve re- FÖ, and EY made eye measurements.SD wrote and edited the manuscript. All authors read and approved the final manuscript. gions in the vitiligo patients. When we reviewed the relevant literature on this subject, we have not seen Ethics approval and consent to participate any published studies that would allow us to make a This study was carried out between 2015 and 2016 in accordance with the tenets of the Declaration of Helsinki. The study protocol was approved by direct comparison regarding our findings. The lack of the Local Ethical Committee of the University of Kırıkkale. All patients and differences between the vitiligo patients and the con- control subjects voluntarily participated in this study and signed an informed trol groupinoptic nerveregions maybebecause me- consent form. lanocytes occupy less space in the histological Competing interests structure in the optic nerve regions. The authors declare that they have no competing interests. Some studies maintained that gender and hormonal status may influence choroidal blood flow and lead to Publisher’sNote change in the choroidal thickness [26, 27]. However, in Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. our study, it was observed that gender resulted the dif- ference in choroidal thickness neither in the vitiligo pa- Author details tients group nor the control group. Department of Dermatology and Venerology, Kirikkale University Faculty of Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, Many authors have reported that the reasons for the Turkey. Department of Ophtalmology, Kirikkale University Faculty of differences in the choroidal thickness results between Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, studies are different software programs for measure- Turkey. ment, differences in the light source of the OCT, ethnic Received: 14 December 2017 Accepted: 23 May 2018 differences, differences in the age, refraction defects and axial length in the patient profile [14–20]. However, since a comparison was made with the control group, References 1. Alikhan A, Felsten LM, Daly M, Petronic-Rosic V. Vitiligo: a comprehensive and the characteristics of the patient and control group overview part I. Introduction, epidemiology, quality of life, diagnosis, were similar, the findings suggest that comparison of the diferantial diagnosis, associations, histopathology, etiology, andwork-up. J measurements resulted in useful data. Am Acad Dermatol. 2011;65(3):473–91. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 6 of 6 2. Ortonne JP, Passeron T. Vitiligo and other disorders of hypopigmentation. In: Bolognia JL, Jorizzo JL, Scaheffer JV, editors. Dermatology. 3rd ed. Philedelphia: Elsevier Saunders; 2012. p. 1023–30. 3. Taieb A, Alomar A, Böhm M, Dell’anna ML, De Pase A, Eleftheriadou V, et al. Guidelines for the management of vitiligo: the European dermatology forum consensus. Br J Dermatol. 2013;168(1):5–19. 4. Ryan SJ. Retina, vol. 1. 4th ed. Philadelphia: Elsevier Mosby; 2006. 5. Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res. 2010; 29:144–68. 6. Chung SE, Kang SW, Lee JH, et al. Choroidal thickness in polypoidal choroidal vasculopathy and exudative age-related macular degeneration. Ophthalmology. 2011;118:840–5. 7. Kurt A, Kurt EE, Kılıç R, Öktem C, Tuncay F, Erdem HR. Is choroidal thickness related with disease activity and joint damage in patient with rheumatoid arthritis. Bratisl Lek Listy. 2017;118(1):23–7. 8. Kılıç R, Kurt A, Acer E, Öktem Ç, Kocamış Ö. Choroidal thickness in psoriasis. Int Ophthalmol. 2017;37(1):173–7. 9. Kola M, Kalkisim A, Karkucak M, et al. Evaluation of choroidal thickness in ankylosing spondylitis using optical coherence tomography. Ocul Immunol Inflamm. 2014;22:434–8. 10. Örnek N, Onaran Z, Koçak M, Örnek K. Retinal nerve fiber layer thickness in vitiligo patients. J Res Med Sci. 2013;18(5):405–7. 11. Hamzavi I, Jain H, McLean D, Shapiro J, Zeng H, Lui H. Parametric modeling of narrowband UV-B phototherapy for vitiligo using a novel quantitative tool: the vitiligo area scoring index. Arch Dermatol. 2004;140(6):677–83. 12. Ikuno Y, Kawaguchi K, Nouchi T, Yasuno Y. Choroidal thickness in healthy Japanese subjects. Invest Ophthalmol Vis Sci. 2010;51:2173–6. 13. Agawa T, Miura M, Ikuno Y, Makita S, Fabritius T, Iwasaki T, et al. Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol. 2011;249(10):1485–92. 14. Yiu G, Chiu SJ, Petrou PA, Stinnett S, Sarin N, Farsiu S, et al. Relationship of central choroidal thickness with age-related macular degeneration status. Am J Ophthalmol. 2015;159(4):617–26. 15. Sanchez-Cano A, Orduna E, Segura F, Lopez C, Cuenca N, Abecia E, Pinilla I. Choroidal thickness and volume in healthy young white adults and the relationships between them and axial length, ammetropy and sex. Am J Ophthalmol. 2014;158(3):574–83. 16. Akay F, Gundogan FC, Yolcu U, Toyran S, Uzun S. Choroidal thickness in systemic arterial hypertension. Eur J Ophthalmol. 2016;26(2):152–7. 17. Sizmaz S, Küçüker Dönmez C, Pinarci EY, Karalezli A, Canan H, Yilmaz G. The effect of smoking on choroidal thickness measured by optical coherence tomography. Br J Ophthalmol. 2013;97:601–4. 18. Duru N, Altinkaynak H, Erten Ş, Can ME, Duru Z, Uğurlu FG, ÇağılN. Thinning of choroidal thickness in patients with rheumatoid arthritis unrelated to disease activity. Ocul Immunol Inflamm. 2015;31:1–8. 19. Ingegnoli F, Gualtierotti R, Pierro L, Del Turco C, Miserocchi E, Schioppo T, ACUTE study group, et al. Choroidal impairment and macular thinning in patients with systemic sclerosis: the acute study. Microvasc Res. 2015;97:31–6. 20. Pekel G, Alur I, Alihanoglu YI, Yagci R, Emrecan B. Choroidal changes after cardiopulmonary bypass. Perfusion. 2014;29:560–6. 21. Karabas L, Esen F, Celiker H, Elcioglu N, Cerman E, Eraslan M, Kazokoglu H, Sahin O. Decreased subfoveal choroidal thickness and failure of emmetropisation in patients with oculocutaneous albinism. Br J Ophthalmol. 2014;98:1087–90. 22. Bordaberry MF. Vogt-Koyanagi-Harada disease: diagnosis and treatments update. Curr Opin Ophthalmol. 2010;21:430–5. 23. Nakayama M, Keino H, Okada AA, Watanabe T, Taki W, Inoue M, Hirakata A. Enhanced depth imaging optical coherence tomography of the choroid in Vogt-Koyanagi-Harada disease. Retina. 2012;32:2061–9. 24. Bulbul-Baskan E, Baykara M, Ercan İ, Tunali S, Yucel A. Vitiligo and ocular findings: a study on possible associations. J Eur Acad Dermatol Venereol. 2006;20:829–33. 25. Ayotunde A, Olakunle G. Ophthalmic assessment in black patients with vitiligo. J Natl Med Assoc. 2005;97(2):286–7. 26. Kavroulaki D, Gugleta K, Kochkorov A, et al. Influence of gender and menopausal status on peripheral and choroidal circulation. Acta Ophthalmol. 2010;88:850–3. 27. Centofanti M, Bonini S, Manni G. Do sex and hormonal status influence choroidal circulation? Br J Ophthalmol. 2000;84:786–7. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png BMC Ophthalmology Springer Journals

Decreased choroidal thickness in vitiligo patients

Free
6 pages

Loading next page...
 
/lp/springer_journal/decreased-choroidal-thickness-in-vitiligo-patients-tAxUTVaUK6
Publisher
BioMed Central
Copyright
Copyright © 2018 by The Author(s).
Subject
Medicine & Public Health; Ophthalmology
eISSN
1471-2415
D.O.I.
10.1186/s12886-018-0796-0
Publisher site
See Article on Publisher Site

Abstract

Background: Vitiligo is a disease characterized by depigmented macules and patches that occur as a result of the loss of functional melanocytes from the affected skin through a mechanism which has not been elucidated yet. Destruction of pigment cells in vitiligo may not remain limited to the skin; the eyelashes, iris, ciliary body, choroid, retinal pigment epithelium and meninges may also be affected. This study aims to compare the choroidal thickness of patients with and without vitiligo using optical coherence tomography (OCT). Methods: Spectral-domain optical coherence tomography (SD-OCT) (Retina Scan Advanced RS-3000 NIDEK, Japan) instrument (with λ = 840 nm, 27,000 A-scans/second and 5 μm axial resolution) was used for the imaging. Statistical analysis was performed using SPSS 21.0 software package. Results: In all values except optic nevre area measurements, the choroidal thickness of all vitiligo patients was found out to be thinner compared to the control group. Conclusions: In vitiligo, the choroidal thickness may be affected by the loss of melanocytes. Keywords: Vitiligo, Choroidal thickness, OCT, VASI, Oculocutaneous disease Background large-caliber vessels (known as Sattler’sand Haller’s Vitiligo is a disease characterized by depigmented layers, respectively), and a suprachoroidal layer, all macules and patches that occur as a result of the loss embedded within a collagenous and elastic stroma of functional melanocytes from the affected skin along with melanocytes [5]. The choroidal changes in through a mechanism which has not been elucidated many ocular pathological conditions such as polypoi- yet. The frequency of vitiligo throughout the world dal choroidal vasculopathy and age related macular changes in the rate of 0.5–2% and does not vary degeneration were reported [6]. Choroidal thickness depending on gender and race [1–3]. While vitiligo changes has also previously been observed in many may occur at all ages soon after birth, the average systemic inflammatory disorders [6–9]. age of onset is approximately 20 years [1–3]. Melanocytes in the eyes consist of neural crest cells The choroid is a vascularized and pigmented tissue that have migrated ventrally. These melanocytes are which was first examined histologically in the 17th located in the uveal tract (choroid, ciliary body, and century and then tried to be visualized by various the iris). Especially the stroma of the choroid layer methods [4]. The choroid of the eye is a highly consists of a high number of melanocytes [5]. The vascularized structure that supplies the outer retina melanin, which is produced in melanocytes in the and, histologically, consists of a thin choriocapillaris choroid layer, has an important function in an area layer that is adjacent to the retinal pigment epithe- starting from the retina and extending to the visual lium (RPE) and Bruch’s membrane, medium- and cortex of the brain. Melanin, which is produced in melanocytes in the eye and stored in melanosomes, * Correspondence: serkan.demirkan@yahoo.com.tr has a very important role in the protection of the eye Department of Dermatology and Venerology, Kirikkale University Faculty of from the intraocular reflections of the light [5]. Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, Turkey Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 2 of 6 Destruction of pigment cells in vitiligo may not remain diabetes, cigarette use, hypertension, antihypertensive limited to the skin; the eyelashes, iris, ciliary body, chor- drug use, known atherosclerotic disease, pregnancy, oid, retinal pigment epithelium and meninges may also macular degenerations, previous ocular surgery, choroidal be affected [10]. Low choroidal thickness may be ex- pathology, glaucoma, high refractive error (patients with pected in vitiligo where melanocyte loss proceeds [10]. more than + 6 and −6 diopters as cycloplegic spherical Although there have been many studies conducted to equivalent), best corrected visual acuity below 20/25, and evaluate choroidal thickening in diseases that affected patients with a systemic other disease were not in- eye vasculature, limited research has been conducted on cluded in this study. Spectral-domain optical coher- the diseases that affect melanocytes and another compo- ence tomography (SD-OCT) (Retina Scan Advanced nent of choroidal tissue, which remained under-researched. RS-3000 NIDEK, Japan) instrument (with λ = 840 nm, This study aims to compare the choroidal thickness of 27,000 A-scans/second and 5 μm axial resolution) patients with and without vitiligo using optical coher- was used for the imaging. ence tomography (OCT). Before evaluation, using EDI-OCT scanning, the cen- tral macular thickness was measured in the right eye of Methods each patient. Choroidal and scleral boundaries were This prospective clinical study addresses the examin- drawn with the assistance of software programs. Chor- ation of the bilateral eyes of (154 eyes). A total of 77 in- oidal thickness was measured at the center of the fovea dividuals, including 34 vitiligo and 43 non-vitiligo, were (SubF), and 500 μm nasally, temporally, superiorly and included in the study. This study was carried out be- inferiorly (N1, T1, S1, I1), and 1500 μm (N2, T2, S2, I2) tween 2015 and 2016 in accordance with the tenets of from the center of the fovea. The peripapillary region the Declaration of Helsinki. The study protocol was ap- was measured 500 μm (N, T, S, I) from the center of proved by the Local Ethical Committee of the University the optic nerve. The averages of upper hemifield, lower of Kırıkkale. All patients and control subjects voluntarily hemifield, and whole hemifield of the peripapillary re- participated in this study and signed an informed con- gion were also measured (Fig. 1a, b). The foveal and sent form. parafoveal choroidal thickness was determined by Patients, who were diagnosed with vitiligo and were measuring the region between the outer border of the aged between 20 and 50 years, and non-vitiligo adults retinal pigment epithelium layer and the sclero-choroidal with similar characteristics participated in this study. interface manually. Measurements in the peripapillary VASI (vitiligo area severity index), which shows the de- area were carried out automatically with the instrument. pigmentation extent, was calculated in all vitiligo pa- The values of the right and left eyes of the patient and tients [11]. The percentage of the body area involved can control group were separately specified and compared. All be estimated by the so-called 1% rule or “palm method”. measurements are presented with median, minimum and In both children and adults, the palm of the hand, in- maximum values. cluding the fingers, is approximately 1% of the total body Statistical analysis was performed using SPSS 21.0 soft- surface area (TBSA), and it describes hand unit [11]. For ware package. Descriptive statistics were presented as a each body region, the VASI was determined by the prod- mean ± standard deviation. In comparisons between pa- uct of the area of vitiligo in hand units and the extent of tient and control groups, the student’s t-test was applied depigmentation within each hand unit–measured patch to numerical data that followed a normal distribution, (possible values of 0, 10, 25, 50, 75, 90% or 100%). The while the Mann-Whitney U test was applied to data total body VASI was calculated using the following for- that did not follow a normal distribution. The Pearson mula considering the contributions of all body regions correlation test was applied to normally distributed (possible range, 0–100): measurements, and the Spearman correlation test was applied to data that did not follow a normal distribu- VASI ¼ All Body Sites½ Hand Units tion. The statistical significance value was accepted as p <0.05. ½ Residual Depigmentation All participants had a thorough ophthalmologic exam- Results ination, uncorrected visual acuity, best corrected visual Thirty four vitiligo patients and 43 individuals without acuity, manifest refraction, cycloplegic refraction and vitiligo diagnosis were included in the study. The mean slit-lamp examination. Intraocular pressures were mea- age of the vitiligo patients was 39.2 years, and the aver- sured with an air-puff tonometer. Dilated fundus exami- age age of the individuals in the control group was nations were performed using a 78 D lens. 39.3 years. Table 1 shows the age and sex distrubation, Individuals with poor OCT quality having a history intraocular pressure, axial length, visual acuity, and re- that may have affected the choroidal thickness, such as fraction defect values of the patients and control group. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 3 of 6 Fig. 1 a, b The areas of choroidal thickness measurements In all values except optic nerve area measurements, Discussion the choroidal thickness of all vitiligo patients was found The stroma of the choroid layer consists of a high num- out to be thinner compared to the control group ber of melanocytes [5]. Destruction of pigment cells in (Table 2). Correlation between VASI values of vitiligo vitiligo may not remain limited to the skin; the eye- patients and age, duration of disease, and choroidal lashes, iris, ciliary body, choroid, retinal pigment epithe- thickness were signed in Table 3. lium and meninges may also be affected [10]. A low There was a negative correlation between age and choroidal thickness may be expected in vitiligo where choroidal thickness in some areas in patients. In pa- melanocyte loss proceeds [10]. To our knowledge, this is tients and control groups, gender had an effect on the first study that examined the relation between chor- the choroidal difference in none of the measured oidal changes and vitiligo in adulthood. regions (p > 0.05). There was no correlation between The choroid covers the outer retina and is among the duration of disease and choroidal thickness in all most vascularized tissues in the body. This tissue sup- areas. plies oxygen and nutrition to and provides temperature In those with higher VASI value, periorbital involve- regulation for the retina. Also, choroid-containing me- ment was significantly more frequent. (p = 0.029). lanocytes prevent intraocular reflections. In the eye, The frequency of periorbital involvement increased choroidal thickness may be affected by several factors, with the duration of the disease (p < 0.001). The peri- such as age, axial length, and refractive errors [12, 13]. orbital involvement did not have an effect on chor- A number of studies have found that choroidal thick- oidal thickness in patients with vitiligo. There was no ness plays a prognostic or predictive role in various statistically significant difference between those with local (e.g., diabetic retinopathy), and systemic diseases and without periorbital involvement concerning age (e.g., hypertension, anemia, rheumatoid arthritis and (p = 0.300). obesity) [14–20]. Table 1 Age and sex distrubation, intraocular pressure, axial length, visual acuity, refraction defect values of the patients and control group Patients (n:34) Control group (n:43) P value (mean±) (mean±) Age 39.2 ± 16.14 39.3 ± 12.51 0.101* Sex(F/M) 15:19 (44%:56%) 20:23 (46%:54%) Right intraocular pressures 14.20 ± 3.31 15.00 ± 2.23 0.105* Left intraocular pressures 14.55 ± 2.83 14.76 ± 2.09 0.347* Axial length 23.57 ± 1.04 23.58 ± 1.22 0.960* Right eyes visual acuity 0.07 ± 0.21 −0.01 ± 0.26 0.330* Left eyes visual acuity 0.08 ± 0.22 0.06 ± 0.40 0.845* Right eye refraction defect − 0.37 ± 1.00 0.00 ± 0.92 0.184* Left eyes refraction defect −0.21 ± 0.97 − 0.01 ± 0.98 0.702* *…Student’s t test Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 4 of 6 Table 2 Mean choroidal thickness in vitiligo patients and control group individuals Patient (n:34) Control (n:43) P value Mean ± SD Minimum Median Maximum Mean ± SD Minimum Median Maximum Right, SubF 220.2 ± 39.8 170 224 290 261.4 ± 31.1 168 256 305 < 0.001** Right, N1 223.6 ± 42.1 163 220 276 258.4 ± 32.5 190 248 302 < 0.001** Right, N2 226.0 ± 39.2 130 220 340 261.5 ± 37.4 200 265 361 < 0.001* Right, T1 220.5 ± 39.9 143 224 303 257.9 ± 34.2 139 257.5 311 < 0.001** Right, T2 225.2 ± 41.1 109 220 280 253.4 ± 32.3 200 250 327 0.001* Right, S1 222.9 ± 44.6 142 219 296 268.7 ± 38.1 198 271 289 < 0.001** Right, S2 217.8 ± 40.8 151 219 301 259.1 ± 33.4 201 261 306 < 0.001** Right, I1 223.4 ± 45.2 119 221 289 266.3 ± 37.0 136 264 321 < 0.001** Right, I2 224.5 ± 45.2 117 226 340 265.9 ± 34.9 200 260 360 < 0.001* Right optic nerve, LowH 95.0 ± 15.4 34 96 138 97.5 ± 7.9 80 97 118 0.429* Right optic nerve, UpH 80.2 ± 16.8 43 81 128 77.1 ± 16.8 41 79 135 0.418** Right optic nerve, WholP 98.9 ± 15.2 47 97 134 100.5 ± 8.1 54 101 126 0.805* Right optic nerve, N 80.2 ± 16.8 54 77.5 126 77.1 ± 16.8 33 75 117 0.418** Right optic nerve, T 68.9 ± 14.1 45 68 104 68.4 ± 15.5 29 69 99 0.689* Right optic nerve, S 128.9 ± 25.3 59 132 168 129.4 ± 16.5 95 129 175 0.712* Right optic nerve, I 118.9 ± 23.6 21 125.5 175 125.6 ± 17.0 79 125 165 0.230* Left, SubF 222.7 ± 37.3 118 223 296 269.1 ± 31.0 129 267 305 < 0.001** Left, N1 223.7 ± 38.5 105 224 301 271.7 ± 36.1 119 269 301 < 0.001** Left, N2 228.2 ± 39.6 106 227 298 265.4 ± 35.8 129 267 311 < 0.001** Left, T1 227.2 ± 42.2 164 226.5 380 308.2 ± 30.8 210 265 291 < 0.001* Left, T2 235.4 ± 38.3 131 234 324 272.7 ± 35.7 176 275 329 < 0.001** Left, S1 215.3 ± 40.2 126 216 305 257.2 ± 35.2 161 254 298 < 0.001** Left, S2 220.0 ± 37.6 137 219 299 249.5 ± 48.2 148 251 324 0.005** Left, I1 216.5 ± 38.0 139 218 301 262.3 ± 31.7 167 264 341 < 0.001** Left, I2 222.2 ± 37.1 170 220 344 262.8 ± 31.9 210 260 350 < 0.001* Left optic nerve, LowH 94.8 ± 12.2 59 95 141 95.5 ± 11.0 48 97 173 0.955* Left optic nerve, UpH 122.6 ± 19.5 75 96 124 127.3 ± 16.3 77 93 125 0.255** Left optic nerve, WholP 98.1 ± 12.0 70 99 125 100.2 ± 11.7 79 101 133 0.655* Left optic nerve, N 75.6 ± 21.6 30 78 126 82.1 ± 23.7 27 78 174 0.432* Left optic nerve, T 66.0 ± 18.1 35 61.5 106 65.0 ± 14.3 38 66 95 0.782* Left optic nerve, S 128.4 ± 19.9 81 131.5 162 128.6 ± 20.5 76 131 178 0.951* Left optic nerve, I 122.6 ± 19.5 89 122 169 127.3 ± 16.3 97 127 174 0.310* *…Mann Whitney U test **…Student’s t test In oculocutaneous albinism patients with melano- Vogt-Koyanagi-Harada Diseaseis a bilateral granu- cyte absence, the choroidal thickness in the subfoveal lomatous panuveitis associated with autoimmunity de- area was found to be significantly lower compared to veloped against melanocytes [22]. Patients with VKH the control group. However, no difference was found increased choroidal thickness, which is probably due to in the peripapillary region compared to the control exudation with inflammatory processes [23]. Invitiligo group [21]. Choroidal thickness measurement was patients, the inflammatory process is chronic and exuda- compared in a much higher number of regions in our tive is not observed. Therefore, despite the presence of study compared to the aforementioned study in which melanocyte destruction as it is in VKH, the increase in the lower choroidal thickness is also expected in choroidal thickness of vitiligo patients is not expected. vitiligo, which is another disease that proceeds with The study conducted by Bulbul-Baskan et al. showed melanocyte loss [21]. that eye pathology was observed in 10 of the 45 vitiligo Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 5 of 6 Table 3 Correlation between VASI values of vitiligo patients and Conclusion age, duration of disease, and choroidal thickness Melanin, which is produced in melanocytes in the eye VASI r p and stored in melanosomes, has a very important role in the protection of the eye from the intraocular reflections Age Weak correlation 0.349 0.043 of light. In this study, in all values except optic nerve Duration of disease Moderate correlation 0.555 < 0.001 area measurements, the choroidal thickness of all vitiligo Right fovea, horizontal Negative correlation −0.417 0.014 patients was found out to be thinner compared to the Right nasal 500 Negative correlation − 0561 0.001 control group. Right nasal 1500 Negative correlation −0.381 0.026 The melanocyte amount in the choroidal layer in Left fovea, vertical Negative correlation −0.437 0.010 vitiligo should be studied in the future postmortem and in vivo studies. Left superior 500 Negative correlation −0.481 0.004 Left inferior 500 Negative correlation −0.484 0.004 Abbreviations CT: Choroidal thickness; EDI-OCT: Enhanced-depth imaging optical Left superior 1500 Negative correlation −0.356 0.039 coherence tomography; I: Choroidal thickness at 500 μm inferior to the Left inferior 1500 Negative correlation −0.380 0.027 fovea; I1: Choroidal thickness at 500 μm inferior to the fovea; I2: Choroidal thickness at 1500 μm inferior to the fovea; LowH: LowerHemifield; …Pearson correlation test N: Choroidal thickness at 500 μm nasal to the fovea; N1: Choroidal thickness Spearman correlation test at 500 μm nasal to the fovea; N2: Choroidal thickness at 1500 μm nasal to the fovea; OCT: Optical coherence tomography; RPE: Retinal pigment patients. Their findings revealed that iris involvement epithelium; S: Choroidal thickness at 500 μm superior to the fovea; in one patient, ring-like peripapillary atrophy around S1: Choroidal thickness at 500 μm superior to the fovea; S2: Choroidal the optic nerve in seven patients, hyperpigmented rim thickness at 1500 μm superior to the fovea; SD-OCT: Spectral-domain optical coherence tomography; SubF: Choroidal thickness at fovea; T: Choroidal in the left top segment of the retinal pigment epithe- thickness at 500 μm temporal to the fovea; T1: Choroidal thickness at lium in addition to peripapillary atrophy in one patient, 500 μm temporal to the fovea; T2: Choroidal thickness at 1500 μm temporal focal hypopigmented dots in the temporal retinal area to the fovea; UpH: Upper Hemifield; VASI: Vitiligo area severity index; VKH: Vogt-Koyanagi-Harada; WholP: Whole peripapillary in one patient, and diffuse hypopigmentation in onepa- tient were observed [24]. Another study carried out Availability of data and materials with black patients with vitiligo, thin and dot-like pig- The data sets used and/or analysed during the current study are available from the corresponding author on reasonable request. mentary disturbances were identified in four of the 17 patients [25]. Authors’ contributions In the current study, we observed a significant re- SD, GS, ÖGand AAK collected patients and control group for the study.ZO, duction in OCT in all areas except optic nerve re- FÖ, and EY made eye measurements.SD wrote and edited the manuscript. All authors read and approved the final manuscript. gions in the vitiligo patients. When we reviewed the relevant literature on this subject, we have not seen Ethics approval and consent to participate any published studies that would allow us to make a This study was carried out between 2015 and 2016 in accordance with the tenets of the Declaration of Helsinki. The study protocol was approved by direct comparison regarding our findings. The lack of the Local Ethical Committee of the University of Kırıkkale. All patients and differences between the vitiligo patients and the con- control subjects voluntarily participated in this study and signed an informed trol groupinoptic nerveregions maybebecause me- consent form. lanocytes occupy less space in the histological Competing interests structure in the optic nerve regions. The authors declare that they have no competing interests. Some studies maintained that gender and hormonal status may influence choroidal blood flow and lead to Publisher’sNote change in the choroidal thickness [26, 27]. However, in Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. our study, it was observed that gender resulted the dif- ference in choroidal thickness neither in the vitiligo pa- Author details tients group nor the control group. Department of Dermatology and Venerology, Kirikkale University Faculty of Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, Many authors have reported that the reasons for the Turkey. Department of Ophtalmology, Kirikkale University Faculty of differences in the choroidal thickness results between Medicine, Yenisehir District, Tahsin Duru Avenue, No:14, Yahsihan, Kirikkale, studies are different software programs for measure- Turkey. ment, differences in the light source of the OCT, ethnic Received: 14 December 2017 Accepted: 23 May 2018 differences, differences in the age, refraction defects and axial length in the patient profile [14–20]. However, since a comparison was made with the control group, References 1. Alikhan A, Felsten LM, Daly M, Petronic-Rosic V. Vitiligo: a comprehensive and the characteristics of the patient and control group overview part I. Introduction, epidemiology, quality of life, diagnosis, were similar, the findings suggest that comparison of the diferantial diagnosis, associations, histopathology, etiology, andwork-up. J measurements resulted in useful data. Am Acad Dermatol. 2011;65(3):473–91. Demirkan et al. BMC Ophthalmology (2018) 18:126 Page 6 of 6 2. Ortonne JP, Passeron T. Vitiligo and other disorders of hypopigmentation. In: Bolognia JL, Jorizzo JL, Scaheffer JV, editors. Dermatology. 3rd ed. Philedelphia: Elsevier Saunders; 2012. p. 1023–30. 3. Taieb A, Alomar A, Böhm M, Dell’anna ML, De Pase A, Eleftheriadou V, et al. Guidelines for the management of vitiligo: the European dermatology forum consensus. Br J Dermatol. 2013;168(1):5–19. 4. Ryan SJ. Retina, vol. 1. 4th ed. Philadelphia: Elsevier Mosby; 2006. 5. Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res. 2010; 29:144–68. 6. Chung SE, Kang SW, Lee JH, et al. Choroidal thickness in polypoidal choroidal vasculopathy and exudative age-related macular degeneration. Ophthalmology. 2011;118:840–5. 7. Kurt A, Kurt EE, Kılıç R, Öktem C, Tuncay F, Erdem HR. Is choroidal thickness related with disease activity and joint damage in patient with rheumatoid arthritis. Bratisl Lek Listy. 2017;118(1):23–7. 8. Kılıç R, Kurt A, Acer E, Öktem Ç, Kocamış Ö. Choroidal thickness in psoriasis. Int Ophthalmol. 2017;37(1):173–7. 9. Kola M, Kalkisim A, Karkucak M, et al. Evaluation of choroidal thickness in ankylosing spondylitis using optical coherence tomography. Ocul Immunol Inflamm. 2014;22:434–8. 10. Örnek N, Onaran Z, Koçak M, Örnek K. Retinal nerve fiber layer thickness in vitiligo patients. J Res Med Sci. 2013;18(5):405–7. 11. Hamzavi I, Jain H, McLean D, Shapiro J, Zeng H, Lui H. Parametric modeling of narrowband UV-B phototherapy for vitiligo using a novel quantitative tool: the vitiligo area scoring index. Arch Dermatol. 2004;140(6):677–83. 12. Ikuno Y, Kawaguchi K, Nouchi T, Yasuno Y. Choroidal thickness in healthy Japanese subjects. Invest Ophthalmol Vis Sci. 2010;51:2173–6. 13. Agawa T, Miura M, Ikuno Y, Makita S, Fabritius T, Iwasaki T, et al. Choroidal thickness measurement in healthy Japanese subjects by three-dimensional high-penetration optical coherence tomography. Graefes Arch Clin Exp Ophthalmol. 2011;249(10):1485–92. 14. Yiu G, Chiu SJ, Petrou PA, Stinnett S, Sarin N, Farsiu S, et al. Relationship of central choroidal thickness with age-related macular degeneration status. Am J Ophthalmol. 2015;159(4):617–26. 15. Sanchez-Cano A, Orduna E, Segura F, Lopez C, Cuenca N, Abecia E, Pinilla I. Choroidal thickness and volume in healthy young white adults and the relationships between them and axial length, ammetropy and sex. Am J Ophthalmol. 2014;158(3):574–83. 16. Akay F, Gundogan FC, Yolcu U, Toyran S, Uzun S. Choroidal thickness in systemic arterial hypertension. Eur J Ophthalmol. 2016;26(2):152–7. 17. Sizmaz S, Küçüker Dönmez C, Pinarci EY, Karalezli A, Canan H, Yilmaz G. The effect of smoking on choroidal thickness measured by optical coherence tomography. Br J Ophthalmol. 2013;97:601–4. 18. Duru N, Altinkaynak H, Erten Ş, Can ME, Duru Z, Uğurlu FG, ÇağılN. Thinning of choroidal thickness in patients with rheumatoid arthritis unrelated to disease activity. Ocul Immunol Inflamm. 2015;31:1–8. 19. Ingegnoli F, Gualtierotti R, Pierro L, Del Turco C, Miserocchi E, Schioppo T, ACUTE study group, et al. Choroidal impairment and macular thinning in patients with systemic sclerosis: the acute study. Microvasc Res. 2015;97:31–6. 20. Pekel G, Alur I, Alihanoglu YI, Yagci R, Emrecan B. Choroidal changes after cardiopulmonary bypass. Perfusion. 2014;29:560–6. 21. Karabas L, Esen F, Celiker H, Elcioglu N, Cerman E, Eraslan M, Kazokoglu H, Sahin O. Decreased subfoveal choroidal thickness and failure of emmetropisation in patients with oculocutaneous albinism. Br J Ophthalmol. 2014;98:1087–90. 22. Bordaberry MF. Vogt-Koyanagi-Harada disease: diagnosis and treatments update. Curr Opin Ophthalmol. 2010;21:430–5. 23. Nakayama M, Keino H, Okada AA, Watanabe T, Taki W, Inoue M, Hirakata A. Enhanced depth imaging optical coherence tomography of the choroid in Vogt-Koyanagi-Harada disease. Retina. 2012;32:2061–9. 24. Bulbul-Baskan E, Baykara M, Ercan İ, Tunali S, Yucel A. Vitiligo and ocular findings: a study on possible associations. J Eur Acad Dermatol Venereol. 2006;20:829–33. 25. Ayotunde A, Olakunle G. Ophthalmic assessment in black patients with vitiligo. J Natl Med Assoc. 2005;97(2):286–7. 26. Kavroulaki D, Gugleta K, Kochkorov A, et al. Influence of gender and menopausal status on peripheral and choroidal circulation. Acta Ophthalmol. 2010;88:850–3. 27. Centofanti M, Bonini S, Manni G. Do sex and hormonal status influence choroidal circulation? Br J Ophthalmol. 2000;84:786–7.

Journal

BMC OphthalmologySpringer Journals

Published: May 29, 2018

References

You’re reading a free preview. Subscribe to read the entire article.


DeepDyve is your
personal research library

It’s your single place to instantly
discover and read the research
that matters to you.

Enjoy affordable access to
over 18 million articles from more than
15,000 peer-reviewed journals.

All for just $49/month

Explore the DeepDyve Library

Search

Query the DeepDyve database, plus search all of PubMed and Google Scholar seamlessly

Organize

Save any article or search result from DeepDyve, PubMed, and Google Scholar... all in one place.

Access

Get unlimited, online access to over 18 million full-text articles from more than 15,000 scientific journals.

Your journals are on DeepDyve

Read from thousands of the leading scholarly journals from SpringerNature, Elsevier, Wiley-Blackwell, Oxford University Press and more.

All the latest content is available, no embargo periods.

See the journals in your area

DeepDyve

Freelancer

DeepDyve

Pro

Price

FREE

$49/month
$360/year

Save searches from
Google Scholar,
PubMed

Create lists to
organize your research

Export lists, citations

Read DeepDyve articles

Abstract access only

Unlimited access to over
18 million full-text articles

Print

20 pages / month

PDF Discount

20% off