Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Optical Coherence Tomography Angiography Findings in Diffuse Unilateral Subacute Neuroretinitis

Luiz H. Lima, MD, PhD; Gustavo B. Melo, MD, PhD; Claudio Zett, MT, PhD; Fábio B. Morais, MD, PhD; Bruno C. Leal, MD, PhD; Michel E. Farah, MD, PhD; Rubens Belfort Jr., MD, PhD

Abstract

BACKGROUND AND OBJECTIVE:

To report a unique case series of diffuse unilateral subacute neuroretinitis (DUSN) patients imaged with optical coherence tomography angiography (OCTA).

PATIENTS AND METHODS:

In this retrospective case series, multimodal imaging was performed in four patients with DUSN at the time of patient visit. The study patients underwent standard clinical treatment for DUSN.

RESULTS:

The clinical findings were consistent with the diagnosis of DUSN. Cross-sectional OCT showed disruption of outer retinal layers in the foveal area and an irregular structure of the outer plexiform layer. En face OCT revealed hyperreflective spots and a large hyperreflective lesion in the foveal area correspondent to the outer retina disruption seen on cross-sectional OCT. OCTA demonstrated decreased vascular perfusion in both the superficial and deep retinal capillary plexuses along with choriocapillaris preservation.

CONCLUSION:

OCTA may provide a more detailed assessment of the retinal microvascular changes, allowing a more precise anatomical-functional correlation in DUSN.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:76–83.]

Abstract

BACKGROUND AND OBJECTIVE:

To report a unique case series of diffuse unilateral subacute neuroretinitis (DUSN) patients imaged with optical coherence tomography angiography (OCTA).

PATIENTS AND METHODS:

In this retrospective case series, multimodal imaging was performed in four patients with DUSN at the time of patient visit. The study patients underwent standard clinical treatment for DUSN.

RESULTS:

The clinical findings were consistent with the diagnosis of DUSN. Cross-sectional OCT showed disruption of outer retinal layers in the foveal area and an irregular structure of the outer plexiform layer. En face OCT revealed hyperreflective spots and a large hyperreflective lesion in the foveal area correspondent to the outer retina disruption seen on cross-sectional OCT. OCTA demonstrated decreased vascular perfusion in both the superficial and deep retinal capillary plexuses along with choriocapillaris preservation.

CONCLUSION:

OCTA may provide a more detailed assessment of the retinal microvascular changes, allowing a more precise anatomical-functional correlation in DUSN.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:76–83.]

Introduction

Diffuse unilateral subacute neuroretinitis (DUSN) was described in 1978 by Gass,1 and the disease usually affects children and young, healthy adults who present with a unilateral and severe loss of peripheral and central visual acuity (VA). DUSN is a rare ocular parasitic disease, and it is typically found in warm and humid endemic areas of developing countries, such as Brazil and India. Although several nematodes have been reported to be related to DUSN etiology, Ancylostoma caninum and Baylisascaris procyonis represent the most common nematodes associated with this disease.2,3

Clinically, DUSN is characterized by vitritis, atrophy of optic disc, retinal vessels narrowing, diffuse retinal pigment epithelium (RPE) mottling, and subnormal electroretinography (ERG). The nematode diagnosis is hampered by the difficulty in identifying the worm on retinal examination and lack of reliable serologic testing. The treatment of DUSN is based on laser photocoagulation addressed to an identified worm or oral antihelminthics if a worm is not found, but there is a substantial suspicion for intraocular worm.4–7

Optical coherence tomography angiography (OCTA) is a functional supplement of OCT and represents a novel, noninvasive imaging technique that provides retinal and choroidal vasculature data by detecting motion contrast from flowing blood. The documentation of erythrocyte movement with several repeated scans results in a microvasculature map that may assess retinal and choroidal diseases more precisely.8,9 In a recent case report of DUSN, the OCTA was able to detect an intraretinal nematode within the macular area. Plausibly, this identification using OCTA was possible due to the worm movement since nematodes have no vascular system.10 The purpose of this case series is to describe the retinal vasculature abnormalities on OCTA findings in patients with early and late stages of presumed DUSN.

Patients and Methods

Case 1

A 9-year-old girl presented to clinic complaining of progressive unilateral decrease of VA in the right eye for 7 months. Although the patient had an unremarkable previous medical and ocular history, a recent contact with animals was reported. Serologies for herpes simplex virus, cytomegalovirus, syphilis, Bartonella species, Toxoplasma gondii, Borrelia burgdorferi, and Toxocara canis were negative. On ocular examination, the best-corrected VA (BCVA) was 20/400 in the right eye and 20/25 in the left eye. Biomicroscopy of the anterior segment, pupillary reactions, and intraocular pressure (IOP) were normal in both eyes, and vitreous cells 1+ were observed in the right eye. Color fundus photograph of the right eye revealed optic disc swelling, retinal vessels tortuosity, diffuse yellowish subretinal infiltrates, and exudation within the macular area. Fluorescein angiography (FA) of the right eye demonstrated areas of hypofluorescence corresponding to the subretinal infiltrates seen on color fundus photograph. Fundus autofluorescence (FAF) of the right eye revealed hypo- and hyperautofluorescent spots in the posterior pole. Cross-sectional OCT (RTVue XR Avanti; Optovue, Fremont, CA) of the right eye showed optic disc edema, disruption of the outer retinal layers in the foveal area, and hyperreflective and irregular points in the outer plexiform layer (OPL) corresponding to the macular exudation seen on color fundus imaging. OCTA of the superficial capillary plexus (SCP), deep capillary plexus (DCP), outer retina, and choriocapillaris depicted absence of vascular perfusion abnormalities in the macular area. En face OCT demonstrated hyperreflective spots within the macular area correspondent to the hyperreflective spots seen in the OPL, as well as a larger hyperreflective lesion correspondent to the outer retina disruption within the foveal area on cross-sectional OCT. En face OCT at the level of the choriocapillaris showed homogeneous reflectivity without artifacts or any other abnormalities (Figure 1). The patient was treated with oral albendazole (Albenza; Amneal Pharmaceuticals, Bridgewater, NJ) 200 mg twice per day.

Case 1. Multimodal imaging of a 9-year-old girl with early stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows optic disc swelling, widespread yellowish subretinal infiltrates, and exudation within the macular area. (B) Reference fundus image demonstrates normal values on the macular thickness map. (C) Fundus autofluorescence depicts hypo- and hyperautofluorescent lesions around both the temporal vascular arcades and optic disc. (D) Cross-sectional optical coherence tomography (OCT) represented by the yellow line in image B shows optic disc edema, disruption of the outer retinal layers in the foveal area (red arrowhead), and hyperreflective and irregular points in the outer plexiform layer (green arrowhead) corresponding to the macular exudation seen on color fundus imaging. Some hyperreflective pinpoints corresponding to inflammatory cells are observed in the vitreous cavity. The amount of these cells is greater around the optic disc. (E, F, G, H) OCT angiography (OCTA) of the superficial capillary plexus (E), deep capillary plexus (F), outer retina (G), and choriocapillaris (H) (represented by the blue square in image B shows absence of vascular perfusion abnormalities in the macular area). (I, J, K, L) En face OCT correspondent to the segmentation performed, respectively, in images E, F, G and H, shows hyporeflective points probably due to the optical attenuation caused by inflammatory cells observed in the vitreous cavity (I), hyperreflective spots within the macular area correspondent to the hyperreflective lesions seen in the outer plexiform layer (J), a hyperreflective lesion correspondent to the lesion observed in the outer retina within the foveal area on cross-sectional OCT (K), and a homogeneous reflectivity without artifacts or any other abnormalities at the level of choriocapillaris (L).

Figure 1.

Case 1. Multimodal imaging of a 9-year-old girl with early stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows optic disc swelling, widespread yellowish subretinal infiltrates, and exudation within the macular area. (B) Reference fundus image demonstrates normal values on the macular thickness map. (C) Fundus autofluorescence depicts hypo- and hyperautofluorescent lesions around both the temporal vascular arcades and optic disc. (D) Cross-sectional optical coherence tomography (OCT) represented by the yellow line in image B shows optic disc edema, disruption of the outer retinal layers in the foveal area (red arrowhead), and hyperreflective and irregular points in the outer plexiform layer (green arrowhead) corresponding to the macular exudation seen on color fundus imaging. Some hyperreflective pinpoints corresponding to inflammatory cells are observed in the vitreous cavity. The amount of these cells is greater around the optic disc. (E, F, G, H) OCT angiography (OCTA) of the superficial capillary plexus (E), deep capillary plexus (F), outer retina (G), and choriocapillaris (H) (represented by the blue square in image B shows absence of vascular perfusion abnormalities in the macular area). (I, J, K, L) En face OCT correspondent to the segmentation performed, respectively, in images E, F, G and H, shows hyporeflective points probably due to the optical attenuation caused by inflammatory cells observed in the vitreous cavity (I), hyperreflective spots within the macular area correspondent to the hyperreflective lesions seen in the outer plexiform layer (J), a hyperreflective lesion correspondent to the lesion observed in the outer retina within the foveal area on cross-sectional OCT (K), and a homogeneous reflectivity without artifacts or any other abnormalities at the level of choriocapillaris (L).

Case 2

A 14-year-old boy presented with decreased VA in the right eye for 2 years. The patient had an unremarkable previous medical and ocular history, but an exposure to animal carriers was reported. Serologies for herpes simplex virus, cytomegalovirus, syphilis, Bartonella, T. gondii, B. burgdorferi, and T. canis were negative. On ocular examination, BCVA was 20/200 in the right eye and 20/20 in the left eye. Biomicroscopy of the anterior segment, pupillary reactions, and IOP were normal in both eyes. Color fundus photograph of the right eye revealed diffuse RPE atrophy, attenuated retinal vessels, and optic disc pallor. FA of the right eye demonstrated widespread hyperfluorescence corresponding to the window defect due to the diffuse RPE atrophy seen on color fundus photograph. FAF of the right eye revealed diffuse hypo- and hyperautofluorescent spots in the fundus. Cross-sectional OCT of the right eye showed retinal atrophy with thinning of the inner nuclear and inner plexiform layers. OCTA 6 mm × 6 mm showed decreased vascular density in the SCP and DCP, and normal vascular perfusion in the choriocapillaris. OCTA 3 mm × 3 mm of the SCP, DCP, and choriocapillaris showed a hypoperfusion area within the foveal area (Figure 2). The patient was treated with oral albendazole (200 mg twice per day).

Case 2. Multimodal imaging of a 14-year-old boy with late-stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium (RPE) atrophy, attenuated retinal vessels, and optic disc pallor. (B) Fluorescein angiography (FA) demonstrates widespread hyperfluorescent spots corresponding to the window defect due to the diffuse RPE atrophy seen on color fundus photograph. (C) Fundus autofluorescence reveals diffuse hypo- and hyperautofluorescent spots in the fundus. (D) Reference fundus image demonstrates decreased values on the macular thickness map. (E) Cross-sectional optical coherence tomography (OCT) shows retinal atrophy with thinning of the inner nuclear and inner plexiform layers. (F, G, and H) OCT angiography (OCTA) 6 mm × 6 mm (represented by the blue square in image D) shows decreased vascular density in the superficial capillary plexus (F) and deep capillary plexus (G), and normal vascular perfusion in the choriocapillaris scan (H). (I) Cross-sectional OCT represented by the blue line in image F shows lack of foveal depression along with retinal atrophy. (J, K, L) OCTA 3 mm × 3 mm (represented by the red square in image D) of superficial capillary plexus (J), deep capillary plexus (K), and choriocapillaris (L) shows a hypoperfusion area in the center of the scans. A segmentation artifact is observed in both images J and L. (M) Cross-sectional OCT represented by the red line in image J depicts a pronounced and diffuse retinal atrophy.

Figure 2.

Case 2. Multimodal imaging of a 14-year-old boy with late-stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium (RPE) atrophy, attenuated retinal vessels, and optic disc pallor. (B) Fluorescein angiography (FA) demonstrates widespread hyperfluorescent spots corresponding to the window defect due to the diffuse RPE atrophy seen on color fundus photograph. (C) Fundus autofluorescence reveals diffuse hypo- and hyperautofluorescent spots in the fundus. (D) Reference fundus image demonstrates decreased values on the macular thickness map. (E) Cross-sectional optical coherence tomography (OCT) shows retinal atrophy with thinning of the inner nuclear and inner plexiform layers. (F, G, and H) OCT angiography (OCTA) 6 mm × 6 mm (represented by the blue square in image D) shows decreased vascular density in the superficial capillary plexus (F) and deep capillary plexus (G), and normal vascular perfusion in the choriocapillaris scan (H). (I) Cross-sectional OCT represented by the blue line in image F shows lack of foveal depression along with retinal atrophy. (J, K, L) OCTA 3 mm × 3 mm (represented by the red square in image D) of superficial capillary plexus (J), deep capillary plexus (K), and choriocapillaris (L) shows a hypoperfusion area in the center of the scans. A segmentation artifact is observed in both images J and L. (M) Cross-sectional OCT represented by the red line in image J depicts a pronounced and diffuse retinal atrophy.

Case 3

A 28-year-old woman presented with decreased VA in the right eye for 6 months. The patient had an unremarkable previous medical and ocular history, and a recent contact with animals, including cats, was reported. Serologies for herpes simplex virus, cytomegalovirus, syphilis, Bartonella, T. gondii, B. burgdorferi, and T. canis were negative. On ocular examination, BCVA was 20/70 in the right eye and 20/25 in the left eye. Biomicroscopy of the anterior segment, pupillary reactions, and IOP were normal in both eyes. Color fundus photograph of the right eye revealed widespread RPE atrophy, significantly attenuated retinal vessels, and optic disc atrophy. FA of the right eye demonstrated widespread hyperfluorescence corresponding to window defect due to diffuse RPE atrophy seen on color fundus photograph. FAF of the right eye revealed widespread hypo- and hyperautofluorescent spots in the fundus. Cross-sectional OCT of the right eye showed retinal atrophy with thinning of the inner nuclear and inner plexiform layers in the macular area. OCTA revealed decreased vascular density in the SCP and DCP and normal vascular perfusion in the choriocapillaris. OCTA of the optic disc demonstrated decreased vascular density in the optic disc head and radial peripapillary capillary plexus (Figure 3). The patient was treated with oral albendazole (200 mg twice per day).

Case 3. Multimodal imaging of a 28-year-old woman with late-stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium atrophy, significantly attenuated retinal vessels, and optic disc atrophy. (B) Cross-sectional optical coherence tomography (OCT) represented by the yellow line in image A shows retinal atrophy with thinning of the inner nuclear and inner plexiform layers. (C, D, E) OCT angiography (OCTA) (represented by the blue square in image A) reveals diffuse decreased vascular density in the superficial capillary plexus (C) and deep capillary plexus (D), and normal vascular perfusion in the choriocapillaris scan (E). (F, G, H) OCTA (represented by the red square in image A) of optic disc demonstrates decreased vascular density in the optic disc head (F) and radial peripapillary capillary plexus (G). The segmentation performed at choriocapillaries (H) does not show any vascular abnormalities.

Figure 3.

Case 3. Multimodal imaging of a 28-year-old woman with late-stage diffuse unilateral subacute neuroretinitis in the right eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium atrophy, significantly attenuated retinal vessels, and optic disc atrophy. (B) Cross-sectional optical coherence tomography (OCT) represented by the yellow line in image A shows retinal atrophy with thinning of the inner nuclear and inner plexiform layers. (C, D, E) OCT angiography (OCTA) (represented by the blue square in image A) reveals diffuse decreased vascular density in the superficial capillary plexus (C) and deep capillary plexus (D), and normal vascular perfusion in the choriocapillaris scan (E). (F, G, H) OCTA (represented by the red square in image A) of optic disc demonstrates decreased vascular density in the optic disc head (F) and radial peripapillary capillary plexus (G). The segmentation performed at choriocapillaries (H) does not show any vascular abnormalities.

Case 4

A 21-year-old woman presented to clinic complaining of progressive decrease of VA in the left eye for 4 months. The patient had an unremarkable previous medical and ocular history, and recent contact with live animals was reported. Serologies for herpes simplex virus, cytomegalovirus, syphilis, Bartonella, T. gondii, B. burgdorferi, and T. canis were negative. On ocular examination, BCVA was 20/20 in the right eye and 20/100 in the left eye. Biomicroscopy of the anterior segment, pupillary reactions, and IOP were normal in both eyes, and vitreous cells 1+ were observed in the left eye. Color fundus photograph of the left eye revealed diffuse RPE atrophy, attenuated retinal vessels, and optic disc pallor. FA of the left eye demonstrated widespread hyperfluorescence corresponding to window defect due to diffuse RPE atrophy seen on color fundus photograph. FAF of the left eye revealed diffuse hypoautofluorescent spots in the fundus. Cross-sectional OCT of the left eye showed retinal atrophy along with an irregular structure of the OPL in the macular area. OCTA showed absence of vascular perfusion abnormalities in both the superficial and deep retinal vascular plexuses and in choriocapillaris. En face OCT revealed an abnormal pattern of imaging probably related to the OPL irregularities (Figure 4). The patient was treated with oral albendazole (200 mg twice per day).

Case 4. Multimodal imaging of a 21-year-old woman with late-stage diffuse unilateral subacute neuroretinitis in the left eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium atrophy, attenuated retinal vessels, and optic disc pallor. (B) Reference fundus image demonstrates normal values on the macular thickness map. (C) Fundus autofluorescence reveals diffuse hypoautofluorescent spots in the fundus. (D) Cross-sectional optical coherence tomography (OCT) represented by the red line in image B shows retinal atrophy along with an irregular outer plexiform layer (red arrowheads). (E, F, G, H) OCT angiography (represented by the blue square in image B) of the superficial capillary plexus (E), deep capillary plexus (F), outer retina (G), and choriocapillaris (H) shows absence of vascular perfusion abnormalities in the macular area. (I, J, K, L) En face OCT correspondent to the segmentation performed, respectively, in images E, F, G, and H, reveals an abnormal pattern of imaging probably related to the outer plexiform layer irregularities seen in image D.

Figure 4.

Case 4. Multimodal imaging of a 21-year-old woman with late-stage diffuse unilateral subacute neuroretinitis in the left eye. (A) Color fundus photograph shows diffuse retinal pigment epithelium atrophy, attenuated retinal vessels, and optic disc pallor. (B) Reference fundus image demonstrates normal values on the macular thickness map. (C) Fundus autofluorescence reveals diffuse hypoautofluorescent spots in the fundus. (D) Cross-sectional optical coherence tomography (OCT) represented by the red line in image B shows retinal atrophy along with an irregular outer plexiform layer (red arrowheads). (E, F, G, H) OCT angiography (represented by the blue square in image B) of the superficial capillary plexus (E), deep capillary plexus (F), outer retina (G), and choriocapillaris (H) shows absence of vascular perfusion abnormalities in the macular area. (I, J, K, L) En face OCT correspondent to the segmentation performed, respectively, in images E, F, G, and H, reveals an abnormal pattern of imaging probably related to the outer plexiform layer irregularities seen in image D.

Discussion

DUSN is considered an uncommon infectious ocular disease, and its prevalence may be higher than that reported in the literature. This is probably related to the variable course of the disorder and the struggle in identifying the causative worm on clinical examination.4 The worm size and speed and the geographic area in which the patient lives constitute important clues for the conjecture of disease etiologies. Although a direct observation of a nematode was not obtained in any of the study patients in the present series, this is not infrequent in DUSN, principally if the infection is due to small nematodes, such as the species of Ancylostoma caninum.5,7 In this present report, each study patient had a history of recent contact with animals in endemic areas and had the usual DUSN clinical feature of retinal yellowish lesions. Patients with DUSN may present two stages of disease. In the early stage of disease, chorioretinitis is the predominant feature, and optic and retinal atrophy represent the main findings of the disease in the late stage.7 In our series, one patient (Case 1) presented with the typical features of early stage, such as swelling of the optic disc and diffuse yellowish subretinal infiltrates, and the other three patients presented with common findings of the late stage of DUSN (eg, diffuse RPE atrophy, attenuated retinal vessels, and optic disc pallor).

This report presents the results of multimodal imaging analyses, including OCTA and en face OCT, in four patients with presumed unilateral DUSN. In our series, as typically described in presumed DUSN patients,11,12 FA demonstrated areas of hypo- or hyperfluorescence in the fundus depending on the presence of subretinal infiltrates or window defect secondary to RPE atrophy, respectively, and FAF revealed widespread hyper- and hypoautofluorescent spots correspondent, respectively, to active and chronic DUSN lesions. The findings of cross-sectional OCT were represented by disruption of outer retinal layers in the foveal area, retinal atrophy with thinning of the inner nuclear and inner plexiform layers, and an irregular structure of the OPL. En face OCT revealed an abnormal pattern of imaging probably related to the OPL irregularity and a large hyperreflective lesion in the foveal area correspondent to the outer retina disruption on cross-sectional OCT. These cross-sectional and en face OCT findings may be a result of the worm movement through all the retinal layers. It has been demonstrated that the worm is able to achieve both the inner and outer retina, not only the subretinal space, and cause lesions in the retinal nerve fiber layer, inner and outer retinal layers, and RPE with retinal thinning and atrophy, probably due to the local toxic effect of the byproducts of the worm.13–17

OCTA is a new diagnostic tool, especially for diseases that cause retinal vascular lesion or neovascularization, allowing a noninvasive assessment and follow-up of retinal tissue damage over time. The present case series demonstrated an unaffected choriocapillaris vasculature and both superficial and deep retinal vascular plexuses damage characterized by decreased vascular perfusion. This vascular injury was more precisely demonstrated by OCTA than the FA. Although OCTA cannot identify typical signs of disease activity as FA does, since it is not able to detect vascular leakage or vessel staining, it may give qualitative information regarding variation of vascular retinal perfusion. Also, OCTA can image the deeper retinal capillary layers due to the absence blocked fluorescence.18 In our series of presumed DUSN, OCTA showed decreased retinal vascular density in the SCP and DCP and normal vascular perfusion in the choriocapillaris. In addition, OCTA of the optic disc demonstrated decreased vascular perfusion in the optic disc head and radial peripapillary capillary plexus in one study patient. Anatomically, within the retinal structure, the superficial vascular plexus is observed in the nerve fiber, ganglion cell, and inner plexiform layers and the deep vascular plexus is observed in the inner nuclear and OPLs.19 The impaired retinal vascular perfusion found in both the superficial and deep retinal vascular plexuses and in the radial peripapillary capillary plexus is possibly related to the chronic and progressive changes in the inner and outer retinal layers caused by direct retinal damage by the worm or toxic retinal reaction. In DUSN, OCT reports have shown the presence of nematodes in both the inner and outer retina, and a direct damage of inner and outer retinal layers have been postulated.15,16 The toxic effect on retinal bipolar cells has also been hypothesized as the mechanism of retinal dysfunction.12 Last year, a case of DUSN reported an intraretinal nematode imaged with OCTA demonstrating the important role of OCTA in understanding the disease process and in identifying the location of the worm, be it subretinal, intraretinal or within the choroid. In addition, it was hypothesized that the worm identification was possible due to the worm movement since nematodes have no vascular system, and an inactive worm would probably not detected on OCTA.10 However, this report did not describe the abnormalities caused by the intraocular nematode in the retinal and choroidal vasculatures. Our case series of DUSN demonstrated vascular abnormalities in both the SCPs and DCPs with preservation of the choriocapillaris.

This report has some limitations, including its limited population and absence of follow-up period and visual function assessment. Further reports with OCTA should help to clarify the precise correlation between the nematode and the vascular changes in the retina of patients diagnosed with DUSN. To the best of our knowledge, this is the first report of OCTA showing vascular abnormalities in both the SCPs and DCPs of DUSN patients. Our case series demonstrates that OCTA is valuable imaging tool that can point out damage to the retinal vasculature and provide further understanding of DUSN pathophysiology. In conclusion, OCTA may provide a more detailed assessment of the retinal microvascular changes, allowing a more precise anatomical-functional correlation in DUSN.

References

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Authors

From the Department of Ophthalmology, Federal University of São Paulo, São Paulo, Brazil (LHL, GBDM, CZ, FBM, MEF, RB); Hospital de Olhos de Sergipe, Aracaju, Brazil (GBDM, FBM); Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile (CZ); and Universidade Tiradentes, Sergipe, Brazil (BCL).

The authors report no relevant financial disclosures.

Address correspondence to Gustavo Barreto Melo, MD, PhD, Rua Campo do Brito, 995 São José, Aracaju, SE, 49020-380, Brazil; e-mail: gustavobmelo@yahoo.com.br.

Received: March 18, 2019
Accepted: August 27, 2019

10.3928/23258160-20200129-02

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