Journal of Men's Health,2023,19(7):71-76 DOI:10.22514/jomh.2023.058
Original Research

Correlative study on retinal microvascular changes and sex hormones in male patients with central serous chorioretinopathy

Mingliang Wang1, Yuanyuan Ren2,*,, Huifen Zheng1, Jiwei Zhang1, Xianbo Zhou1

1Department of Ophthalmology, Hangzhou Lin’an District the First People’s Hospital, 311300 Hangzhou, Zhejiang, China

2Department of Dermatology and Venereal Diseases, Hangzhou Lin’an District the First People’s Hospital, 311300 Hangzhou, Zhejiang, China

*Corresponding Author(s):renyuanyuan3022802@163.com (Yuanyuan Ren)

History Submitted: 28 February 2023 | Accepted: 18 April 2023 | Published: 30 July 2023
Copyright:  ©2023  The Author(s). Published by MRE Press.
This is an open access article under the CC BY 4.0 license (https://creativecommons.org/licenses/by/4.0/).

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Abstract

Central serous chorioretinopathy (CSC) is a disease in which the outer retinal barrier is damaged with high incidence in young adult males. We aimed to analyze the correlations between retinal microvascular changes and sex hormone levels. The vascular density of the superficial retinal capillary plexus (SCP), deep retinal capillary plexus (DCP), foveal avascular zone (FAZ) area, choriocapillary blood flow area, and the subfoveal choroidal thickness (SCT) were investigated by optical coherence tomography angiography (OCTA). We also determined the levels of sex hormones (adrenaline (AD), norepinephrine (NE), dopamine (DA), corticosteroids (Cor), aldosterone (ALD), estradiol (E2) and total testosterone (TT)). The relationship between sex hormone levels and OCTA parameters was then determined. We detected significantly higher levels of NE, Cor and TT in serum from the observation group than in the control group (p < 0.05). Significant correlations were identified between SCT and choriocapillary blood flow area in the affected eyes, contralateral eyes and healthy eyes in the control group (p < 0.05). SCT levels of both eyes in the observation group were higher and the choriocapillary blood flow area was smaller than in the control group. The SCT in affected eyes from the observation group were higher than the contralateral eyes (p < 0.05). The choriocapillary blood flow area was significantly smaller than in the contralateral eyes (p < 0.05). Correlation analysis unveiled that NE, Cor and TT levels were positively correlated with SCT in CSC patients and negatively correlated with choriocapillary blood flow area (p < 0.05). The serum levels of sex hormone levels in male CSC patients were different from those in healthy men of the same age. Our findings suggest that the serum levels of NE, Cor and TT levels may influence the pathogenesis of CSC by affecting SCT thickness and choriocapillary blood flow.

Keywords:Male;Central serous chorioretinopathy;Optical coherence tomography angiography;Sex hormones;Retinal microvascular changes
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Cite this article

Mingliang Wang, Yuanyuan Ren, Huifen Zheng, Jiwei Zhang, Xianbo Zhou. Correlative study on retinal microvascular changes and sex hormones in male patients with central serous chorioretinopathy.Journal of Men's Health,2023,19(7):71-76 DOI:10.22514/jomh.2023.058

1. Introduction

Central serous chorioretinopathy (CSC) is rare in clinical practice and occurs frequently in young adult males. Most patients have a good prognosis, although some patients are prone to the development of chronic CSC which can cause permanent impairment of visual function [1, 2, 3]. Once the outer retinal barrier is damaged, the leakage of fluid from the choriocapillaris through retinal pigment epithelium (RPE) lesions results in retinal neuroepithelial detachment in the macular area combined with focal retinal pigment epithelial detachment. Subsequently, patients experience mild visual loss, darkening of vision, hue changes, and a central relative dark area. Medical research suggests that the pathogenesis of CSC is linked to choroidal vascular hyperpermeability, disruption of the RPE barrier, as well as choroidal dysfunction. At present, the specific pathogenesis of CSC remains unclear but may be associated with multiple factors, including ischemia, infection, inflammation, and immune response; however, there is no strong evidence to support these possibilities [4, 5, 6]. Due to the differences in CSC pathogenesis between genders, the relationship between sex hormones and CSC has become a significant hotspot in research [7].

Optical coherence tomography angiography (OCTA) is a newly developed technique for fundus examination. In contrast with traditional examinations, this technique does not require the injection of contrast agents; it also has included a wider array of indicators, a better safety profile and can provide quantitative data relating to ocular blood flow [8, 9, 10]. In this study, we investigated the relationship between sex hormone levels and OCTA parameters in male CSC patients in attempt to identify factors involved in the pathogenesis of CSC. We found that the serum levels of sex hormones s in male CSC patients were different from those of healthy men of the same age. In addition, alterations in the serum levels of NE, Cor and TT may participate in the development of CSC by affecting SCT thickness and choriocapillary blood flow. Our findings provide new reference guidelines for clinical research.

2. Subjects and methods

2.1 Study subjects

2.1.1 Sample size assessment

First, we considered the required sample size. According to published data, S = 12.37 and δ = 7.31. The following parameters were established for the current study: α = 0.05 (bilateral) tα/2 = 1.96, with a power of 1–β = 0.9, and tβ = 1.282. The following formula was used to determine the sample size; this required 60 cases in each group.

N1=N2=2S2(tα2−tβ)2σ2

2.1.2 Case data

We recruited 60 male patients with CSC patients who were admitted to the hospital as an observation group and 60 males of the same age who passed a health examination without fundus lesions as a control group. The inclusion criteria were as follows: CSC patients who were diagnosed with CSC by fundus photography, optical coherence tomography (OCT), fundus fluorescein angiography (FFA) and other examinations; all with monocular CSC. We also included patients with clinical sudden vision loss, darkening of the vision or hue yellowing, metamorphosis or micropsia and other clinical symptoms. Of the 60 cases, 25 were in the chronic phase and 35 were in the acute phase. The course of disease ranged from 1 day to 6 months, with a mean of 1.12 ± 0.25 months. For inclusion, patients needed to be aged 20 to 45 years and be able to complete the relevant examinations. The exclusion criteria were as follows: patients with hypertension, diabetes and other systemic diseases; previous ocular trauma and surgery; the use of exogenous sex hormones; glaucoma, maculopathy and other ocular lesions.

2.2 Methods

2.2.1 Detection of serum levels of sex hormones

Blood samples were collected from all subjects from 14:00 PM to 17:00 PM. Prior to blood collection, the subjects were required to sit quietly for half an hour, and 5 mL of whole blood was collected from the forearm vein and placed in a vacuum blood collection tube and centrifuged at 4000 r/min for 15 min. The supernatant was placed in a microcentrifuge tube and stored in a freezer at –20 °C. Epinephrine (AD), norepinephrine (NE), dopamine (DA), cortisol (COR), aldosterone (ALD), estradiol (E2) and total testosterone (TT) levels were measured by radioimmunoassay.

2.2.2 OCTA examination

OCT and OCTA examinations were performed by the same ophthalmologist with the Optovue RTVue-XR Avanti instrument (G1214719, Optoveu Inc., Fremont, CA, USA). We used the 6 mm × 6 mm OCT imaging mode for retinal blood flow, and each B scan of the OCT data frame consisted of 304 A scans. Each B scan repeated the OCT angiogram at the same position at least twice. Furthermore, OCTA was performed with the Supervisory Control And Data Acquisition (SSADA) algorithm [10] with a working wavelength of 840 nm and 7000 axial scans per second. After scanning the retinal and choroidal vessels, OCTA can be divided into four layers: the superficial and deep retinal plexus, the outer retina and the choriocapillaris. Data relating to the vessel density of the superficial capillary plexus (SCP), deep capillary plexus (DCP), foveal avascular zone (FAZ) area, and choriocapillary blood flow area of the retina, can be acquired directly from built-in software. We also measured the subfoveal choroidal thickness (SCT); the SCT is the vertical distance from the outside of the subfoveal retinal pigment epithelial layer to the inner surface of the sclera.

2.3 Statistical methods

Data were processed by SPSS 19.0 statistical software (Chengdu Enruiqi Information Co., Ltd. Sichuan, China). (Kolmogorov-Smirnov normality test, Levene’s test for homogeneity of variances were used, and nonparametric tests were utilized for variables that did not fit a normal distribution). Measurement data are presented as (x̄ ± s). The independent sample t-test was used to compare means between the two groups. Pearson’s correlation analysis was used for correlation analysis. p < 0.05 was statistically significant.

3. Results

3.1 Age comparisons

The age of males in the observation group ranged from 20 to 45 years, with a mean age of 35.45 ± 10.13 years. The age of males in the control group ranged from 20 to 43 years, with a mean age of 36.17 ± 10.74 years. There was no significant difference between the two groups in terms of age (t = 0.378, p = 0.706).

3.2 Early hyper-fluorescence and/or leakage of FFA corresponded to changes in OCTA images of the choriocapillaris layer

High blood flow signals were observed in the corresponding areas of fundus fluorescein angiography (FAA) early fluorescence and/or leakage in the affected eyes of CSC patients in OCTA, as shown in Fig. 1.

High blood flow signals in the corresponding areas of fundus fluorescein angiography (FAA) early fluorescence and/or leakage in OCTA.

Fig. 1.High blood flow signals in the corresponding areas of fundus fluorescein angiography (FAA) early fluorescence and/or leakage in OCTA.

3.3 Comparison of sex hormone levels between the observation group and control group

The serum levels of NE, Cor and TT in the observation group were significantly higher than those in the control group (p < 0.05) (Table 1).

Table 1.Comparison of sex hormone levels between the observation group and the control group (ng/mL).
GroupnADNEDACorALDTTE2
Observation group600.85 ± 0.169.78 ± 1.294.25 ± 1.02121.25 ± 16.580.16 ± 0.023.94 ± 0.560.02 ± 0.01
Control group600.90 ± 0.174.53 ± 1.154.37 ± 1.05107.48 ± 17.110.15 ± 0.043.21 ± 0.480.02 ± 0.01
t1.65923.5310.6354.4771.7327.6670.000
p0.100<0.0010.527<0.0010.086<0.0011.000
Note: AD: adrenaline; NE: norepinephrine; DA: dopamine; Cor: corticosteroids; ALD: aldosterone; TT: total testosterone; E2: estradiol.

3.4 Comparison of OCTA parameters between both groups

There were significant relationships between OCTA parameters, SCT and choriocapillary blood flow area between the affected eyes, contralateral eyes, and healthy eyes in the control group (p < 0.05). The levels of SCT in both eyes in the observation group were remarkably higher than that in the control group, and the choriocapillary blood flow area was smaller than in the control group. Furthermore, the SCT levels in the affected eyes of patients in the observation group were significantly higher than their contralateral eyes; in addition, the choriocapillary blood flow was significantly lower than that in their contralateral eyes (p < 0.05) (Table 2).

Table 2.Comparison of OCTA parameters between both groups.
GroupnSCT (μm)SCP vascular density (%)DCP vascular density (%)FAZ area (mm2)Choriocapillary blood flow area (mm2)
Observation group
Affected eyes60473.15 ± 84.4848.35 ± 7.4550.14 ± 5.690.35 ± 0.059.51 ± 1.07
Contralateral eyes60356.89 ± 86.54a48.44 ± 6.5950.31 ± 6.630.34 ± 0.069.72 ± 1.12a
Control group60248.47 ± 56.98ab48.74 ± 7.1450.28 ± 6.110.34 ± 0.0710.97 ± 1.08ab
F127.1530.0500.0130.54531.451
p<0.0010.9510.9870.581<0.001
Note: Compared with affected eyes in observation group. ap < 0.05; compared with the contralateral eyes in observation group, bp < 0.05. SCT: subfoveal choroidal thickness; SCP: superficial capillary plexus; DCP: deep capillary plexus; FAZ: foveal avascular zone.

3.5 Relationship between sex hormone levels and OCTA parameters in CSC patients

Correlation analysis showed that the serum levels of NE, Cor and TT were positively correlated with SCT levels in CSC patients and negatively correlated with choriocapillary blood flow area (p < 0.05) (Table 3).

Table 3.CSC Relationship between sex hormone levels and OCTA parameters in CSC patients.
ParametersSCTSCP vascular densityDCP vascular densityFAZ areaChoriocapillary blood flow area
ADr = 0.135r = 0.155r = 0.127r = 0.112r = 0.151
p > 0.05p > 0.05p > 0.05p > 0.05p > 0.05
NEr = 0.341r = 0.174r = 0.115r = 0.089r = −0.311
p < 0.05p > 0.05p > 0.05p > 0.05p < 0.05
DAr = 0.154r = 0.162r = 0.095r = 0.093r = 0.207
p > 0.05p > 0.05p > 0.05p > 0.05p > 0.05
Corr = 0.366r = 0.127r = 0.083r = 0.211r = 0.158
p < 0.05p > 0.05p > 0.05p > 0.05p > 0.05
ALDr = 0.121r = 0.122r = 0.113r = 0.189r = 0.119
p > 0.05p > 0.05p > 0.05p > 0.05p > 0.05
TTr = 0.357r = 0.117r = 0.117r = 0.203r = −0.325
p < 0.05p > 0.05p > 0.05p > 0.05p < 0.05
E2r = 0.089r = 0.132r = 0.059r = 0.177r = 0.178
p > 0.05p > 0.05p > 0.05p > 0.05p > 0.05
Note: SCT: Subfoveal choroidal thickness; SCP: superficial capillary plexus; DCP: deep capillary plexus; FAZ: foveal avarzone; AD: adrenaline; NE: norepinephrine; DA: dopamine; Cor: corticosteroids; ALD: aldosterone; TT: total testosterone; E2: estradiol.

4. Discussion

CSC is a disease in which the outer retinal barrier is damaged, thus resulting in the leakage of fluid from the choriocapillaris through RPE lesions. Subsequently, this causes retinal neuroepithelial detachment in the macular area combined with focal retinal pigment epithelial detachment. Patients experience several clinical manifestations, including mild visual loss, darkening of vision, hue changes, and central relative dark areas [11, 12, 13, 14]. The incidence of CSC differs significantly between genders and occurs predominantly in men and rarely in women. As clinical research advances, our understanding of CSC has developed from the RPE level to the choroidal level. It is now generally accepted that the pathogenesis of CSC is associated with choroidal vascular hyperpermeability, RPE barrier disruption, and choroidal dysfunction [15, 16]. In FFA examinations, we observed RPE barrier disruption and fluorescein leakage. In addition, ICGA examinations revealed choroidal circulation disorder, vasodilatation and leakage. In this study, we found that high blood flow signals were observed in the corresponding areas of FAA early fluorescence and/or leakage in OCTA, thus suggesting that FAA and OCTA examinations can efficiently detect fluorescein leakage, thus validating our hypothesis [17, 18].

OCTA is a new technique used to examine fundus lesions over recent years. This method can clearly demonstrate the morphological characteristics of superficial choroidal vessels and can quantitatively detect retinal blood flow signals [19, 20]. In the present study, OCTA revealed that the SCT of the affected eyes of CSC patients was significantly thicker than that of the healthy eyes. Previous researchers speculated that SCT thickening may be associated with choroidal vasodilatation, choroidal vascular hyperpermeability, and choroidal interstitial edema; in addition, SCT thickening has also been proven to be an important trigger of choroidal structural and functional changes [21, 22, 23]. Moreover, this study also identified a reduced choriocapillary blood flow area in CSC patients compared to their healthy eyes, thus indicating that in addition to SCT thickness changes, CSC also involves pathological changes such as choriocapillaris injury and reduced blood flow. Notably, in addition to the affected eye, the contralateral eye of CSC patients also showed changes, including SCT thickening and a reduced choriocapillary blood flow area. These data indicate that the pathogenesis of CSC may be correlated with systemic factors.

Previously, researchers have reported that several hormones may play an important role in CSC pathogenesis [24, 25]. In this study, the serum levels of NE, Cor and TT tended to increase in male CSC patients when compared with healthy volunteers of the same age. Mental stress, a strong stress response, and hypertension are all risk factors for CSC. In these physiological states, sympathetic excitability of the human body will increase and secrete substantial amounts of catecholamines, including AD, NE and DA [26]. In this study, the levels of NE and Cor were positively correlated with SCT thickness in the affected eyes of CSC patients. Furthermore, NE was also negatively correlated with choriocapillary blood flow area. Previous research suggested that NE and Cor may lead to the development of CSC by stimulating dopamine receptors in the choroid and enhancing sympathetic nerve activity [27, 28]. Furthermore, RPE cells express androgen receptors. In physiological states, there is a fine balance between male and female hormones. Once this balance is disturbed, the levels of catecholamines and adrenocorticotropic hormone increase due to increasing tissue oxygen supply and the restoration of nitrogen balance, thus promoting dehydrogenase activity in the tricarboxylic acid cycle and the regulation of 2,3 diphosphoglycerate metabolism [29]. In this study, serum TT levels were discovered to be increased in CSC patients and were positively correlated with SCT thickness and negatively correlated with choriocapillary blood flow area in their affected eyes.

However, the results of OCTA examination will be affected by exudation, pigment epithelial detachment, the presence of subretinal fluid and other factors; thus data and images arising from OCTA may be inaccurate. Moreover, the sample size included in this study was small and our analysis only featured a single center; thus, our conclusions may be biased. Therefore, further research, involving larger sample sizes, is now required to fully investigate OCTA.

5. Conclusions

The serum levels of sex hormone in male CSC patients differed from those in healthy men of the same age. In addition, serum levels of NE, Cor and TT may be involved in the development of CSC by affecting SCT thickness and choriocapillary blood flow in patients.

Availability of data and materials

The authors declare that all data supporting the findings of this study are available within the paper and any raw data can be obtained from the corresponding author upon request.

Author contributions

MLW and YYR—designed the study and carried them out; MLW, YYR, HFZ, JWZ and XBZ—supervised the data collection, analyzed the data, interpreted the data, prepared the manuscript for publication and reviewed the draft of the manuscript. All authors have read and approved the manuscript.

Ethics approval and consent to participate

Ethical approval was obtained from the Ethics Committee of Hangzhou Lin’an District the First People’s Hospital (Approval no. 2020001). Written informed consent was obtained from a legally authorized representative for anonymized patient information to be published in this article.

Acknowledgment

Not applicable.

Funding

This research received no external funding.

Conflict of interest

The authors declare no conflict of interest.

References

Rugo HS. Continuing advancements in breast cancer care unraveling the data from the 2020 San Antonio breast cancer symposium. Oncology. 2021; 35: 11–13.

[Google Scholar]

Siwiec-Prościńska J, Prościnski T, Kociecki J, Pecold K. Central serous choroidoretinopathy—the characteristics of the clinical picture and the evaluation of the influence of general conditions at the prognosis and the course of the disease. Metaanalysis. Klin Oczna. 2009; 111: 258–262. (In Polish)

[Google Scholar]

Yu S, Park J, Kim K, Kang M, Kim E. Central serous chorioretinopathy: treatment. Taiwan Journal of Ophthalmology. 2022; 12: 394.

[Google Scholar]

Entezari M, Ramezani A, Yaseri M. Intravitreal bevacizumab for treatment of refractory central serous choroidoretinopathy. Korean Journal of Ophthalmology. 2012; 26: 139.

[Google Scholar]

Wali UK, Al-Kharousi N, Hamood H. Photodynamic therapy with verteporfin for chronic central serous choroidoretinopathy and idiopathic choroidal neovascularization—first report from the sultanate of oman. Oman Medical Journal. 2008; 23: 282–286.

[Google Scholar]

Kanda P, Gupta A, Gottlieb C, Karanjia R, Coupland SG, Bal MS. Pathophysiology of central serous chorioretinopathy: a literature review with quality assessment. Eye. 2022; 36: 941–962.

[Google Scholar]

Spaide RF, Gemmy Cheung CM, Matsumoto H, Kishi S, Boon CJF, van Dijk EHC, et al. Venous overload choroidopathy: a hypothetical framework for central serous chorioretinopathy and allied disorders. Progress in Retinal and Eye Research. 2022; 86: 100973.

[Google Scholar]

Lu B, Chao G, Xie L. Optical coherence tomography angiography in retinitis pigmentosa: a narrative review. Medicine. 2022; 101: e30068.

[Google Scholar]

Borrelli E, Battista M, Sacconi R, Querques G, Bandello F. Optical coherence tomography angiography in diabetes. Asia-Pacific Journal of Ophthalmology. 2021; 10: 20–25.

[Google Scholar]

Müller P, Pfau M, Schmitz-Valckenberg S, Fleckenstein M, Holz F. Optical coherence tomography-angiography in geographic atrophy. Ophthalmologica. 2021; 244: 42–50.

[Google Scholar]

Association WM. World medical association declaration of Helsinki. Ethical principles for medical research involving human subjects. Bulletin of the World Health Organization. 2001; 79: 373.

[Google Scholar]

Jain M, Mohan S, van Dijk EC. Central serous chorioretinopathy: pathophysiology, systemic associations, and a novel etiological classification. Taiwan Journal of Ophthalmology. 2022; 12: 381.

[Google Scholar]

Kaye R, Chandra S, Sheth J, Boon CJF, Sivaprasad S, Lotery A. Central serous chorioretinopathy: an update on risk factors, pathophysiology and imaging modalities. Progress in Retinal and Eye Research. 2020; 79: 100865.

[Google Scholar]

Battaglia Parodi M, Arrigo A, Iacono P, Falcomatà B, Bandello F. Central serous chorioretinopathy: treatment with laser. Pharmaceuticals. 2020; 13: 359.

[Google Scholar]

Lei C, Hua R, Duan J, Zhang M. Retinal pigment epithelium aperture in acute central serous chorioretinopathy: another novel possible pathological mechanism. European Journal of Ophthalmology. 2022; 32: NP103–NP108.

[Google Scholar]

Chronopoulos A, Kakkassery V, Strobel MA, Fornoff L, Hattenbach L. The significance of pigment epithelial detachment in central serous chorioretinopathy. European Journal of Ophthalmology. 2021; 31: 556–565.

[Google Scholar]

Jeon SH, Kim M, Lee J, Roh Y. The effect of selective retina therapy for bevacizumab-resistant chronic central serous chorioretinopathy. Ophthalmologica. 2022; 245: 91–100.

[Google Scholar]

Goel N, Mehta A, Gupta A. Multifocal electroretinography-assisted anatomical and functional evaluation of subthreshold green laser in acute central serous chorioretinopathy. Indian Journal of Ophthalmology. 2021; 69: 2341.

[Google Scholar]

Pichi F, Hay S. Use of optical coherence tomography angiography in the uveitis clinic. Graefe’S Archive for Clinical and Experimental Ophthalmology. 2023; 261: 23–36.

[Google Scholar]

Coffey AM, Hutton EK, Combe L, Bhindi P, Gertig D, Constable PA. Optical coherence tomography angiography in primary eye care. Clinical and Experimental Optometry. 2021; 104: 3–13.

[Google Scholar]

Brinks J, van Dijk EHC, Tsonaka R, Meijer OC, Boon CJF. Sex hormones in males and females with active central serous chorioretinopathy. Ophthalmologica. 2022; 245: 555–562.

[Google Scholar]

Singh SR, Iovino C, Zur D, Masarwa D, Iglicki M, Gujar R, et al. Central serous chorioretinopathy imaging biomarkers. British Journal of Ophthalmology. 2022; 106: 553–558.

[Google Scholar]

Zeng Q, Yao Y, Li S, Yang Z, Qu J, Zhao M. Comparison of swept-source OCTA and indocyanine green angiography in central serous chorioretinopathy. BMC Ophthalmol. 2022; 22: 380.

[Google Scholar]

Schellevis RL, Altay L, Kalisingh A, Mulders TWF, Sitnilska V, Hoyng CB, et al. Elevated steroid hormone levels in active chronic central serous chorioretinopathy. Investigative Ophthalmology & Visual Science. 2019; 60: 3407.

[Google Scholar]

Ulaş F, Uyar E, Tekçe H, Çelebi S. Can hypothyroidism cause acute central serous chorioretinopathy? Seminars in Ophthalmology. 2019; 34: 533–540.

[Google Scholar]

Zhao C, Huang Y, Chen L, Ye S, Liu XQ. The association between circulating sex hormones and central serous chorioretinopathy: a case-control study. Therapeutics and Clinical Risk Management. 2022; 18: 855–865.

[Google Scholar]

Chang YS, Weng SF, Wang JJ, Jan RL. Temporal association between topical ophthalmic corticosteroid and the risk of central serous chorioretinopathy. International Journal of Environmental Research and Public Health. 2020; 17: 9455.

[Google Scholar]

Çiloğlu E, Unal F, Dogan NC. The relationship between the central serous chorioretinopathy, choroidal thickness, and serum hormone levels. Graefe’S Archive for Clinical and Experimental Ophthalmology. 2018; 256: 1111–1116.

[Google Scholar]

Nudleman E, Witmer MT, Kiss S, Williams GA, Wolfe JD. Central serous chorioretinopathy in patients receiving exogenous testosterone therapy. Retina. 2014; 34: 2128–2132.

[Google Scholar]