|Year : 2023 | Volume
| Issue : 1 | Page : 88-93
Clinical and multimodal imaging characteristics of eyes with Vogt–Koyanagi–Harada disease: An Egyptian experience
Mahmood O Mekkawy1, Yousef Ahmed Fouad2, Mohamed Nowara3, Ihab Abdel Aziz4
1 Al Mashreq Eye Center, Cairo, Egypt
2 Al Mashreq Eye Center; Department of Ophthalmology, Ain Shams University Hospitals, Giza, Egypt
3 Al Mashreq Eye Center; Department of Ophthalmology, Electricity Hospital, Cairo, Egypt
4 Al Mashreq Eye Center, Cairo; Vitreoretinal Service, The Memorial Institute for Ophthalmic Research, Giza, Egypt
|Date of Submission||30-Dec-2021|
|Date of Decision||17-Dec-2022|
|Date of Acceptance||12-Jan-2023|
|Date of Web Publication||21-Feb-2023|
Yousef Ahmed Fouad
Al Mashreq Eye Center, 102 El-Sayed El-Merghany Street, Cairo 11774
Source of Support: None, Conflict of Interest: None
| Abstract|| |
BACKGROUND: Vogt–Koyanagi–Harada (VKH) disease is a vision-threatening inflammatory disorder that is challenging in diagnosis and management.
METHODS: Retrospective, record-based analysis of 54 eyes belonging to 27 adult patients that fulfilled the revised diagnostic criteria for VKH between January 2018 and January 2021. Demographic, clinical, and imaging data on presentation and during follow-up visits were collected for each patient. Available imaging studies included B-scan ultrasonography (B-scan US), spectral domain optical coherence tomography (OCT), fundus fluorescein angiography (FFA), and OCT angiography (OCT-A).
RESULTS: The female-to-male ratio was 2.38:1. Nineteen patients (70.37%) presented during an initial attack, while eight patients (29.63%) presented during recurrence. The most commonly presenting sign in the posterior segment was exudative retinal detachment (44 eyes, 81.48%). B-scan US was utilized in 4 eyes (7.41%), OCT was utilized in 48 eyes (88.89%) with the most common finding being subretinal fluid (43 eyes, 89.58%), FFA was performed in 39 eyes (72.22%) with the most common finding being punctate hyperfluorescence and late dye pooling (33 eyes, 84.62%), and OCT-A was performed in 30 eyes (55.56%), in which choriocapillaris flow deficit that correlated with disease activity was detectable in 25 eyes (83.33%). Improved visual acuity was noted in 85% of the eyes that were followed up.
CONCLUSION: Early diagnosis and treatment of VKH result in favorable visual outcome. Multimodal imaging, with the recent addition of OCT-A, provides complementary data that could serve in diagnosis and monitoring.
Keywords: Choroiditis, Harada disease, multimodal imaging, optical coherence tomography angiography, Vogt–Koyanagi–Harada disease
|How to cite this article:|
Mekkawy MO, Fouad YA, Nowara M, Aziz IA. Clinical and multimodal imaging characteristics of eyes with Vogt–Koyanagi–Harada disease: An Egyptian experience. Oman J Ophthalmol 2023;16:88-93
|How to cite this URL:|
Mekkawy MO, Fouad YA, Nowara M, Aziz IA. Clinical and multimodal imaging characteristics of eyes with Vogt–Koyanagi–Harada disease: An Egyptian experience. Oman J Ophthalmol [serial online] 2023 [cited 2023 Mar 26];16:88-93. Available from: https://www.ojoonline.org/text.asp?2023/16/1/88/370055
| Introduction|| |
Vogt–Koyanagi–Harada (VKH) disease is a vision-threatening autoimmune reaction against melanin-associated antigens found in various tissues, most specifically the eyes, ears, skin, and meninges. Although relatively rare, the condition is notably more prevalent in certain populations including Asians, Middle Easterners, native Americans, and Hispanics, which is proposed to be related to genetic risk.
VKH has four clinically consecutive phases: prodromal, acute uveitic, chronic convalescent, and chronic recurrent. Visual symptoms are common as the eye can be affected in multiple stages of the condition. The acute uveitic phase is characterized by bilateral simultaneous or rapidly sequential-posterior uveitis and patients often present in this stage with rapid diminution of vision. The classic clinical features on fundus examination include diffuse choroiditis or chorioretinitis, exudative retinal detachment (ERD), and optic disc swelling. The natural history of VKH in the eye is progression to the convalescent or integumentary phase, in which the hallmark sign is a depigmented choroid described as “sunset glow fundus” (SGF) that may be associated with retinal pigment epithelium (RPE) atrophy and chorioretinal scarring., Recurrence is commonly associated with complications that include cataract, glaucoma, choroidal neovascular membranes (CNV), and subretinal fibrotic bands.
Early recognition and prompt management of VKH during the “therapeutic window” (the initial 2–3 weeks from the onset of the disease) has been shown to significantly limit the progression to SGF and consequently reduce visual morbidity among patients., The widely employed revised diagnostic criteria for VKH classify the presentation of the disease into complete, incomplete, and probable, with bilateral uveitis being a necessary occurrence in all presentations. Consequently, the recognition of early choroiditis – even in subclinical form – is crucial in establishing the diagnosis and preventing disease progression; this has led to the critique directed toward the revised diagnostic criteria which failed to include ocular imaging modalities that characterize stromal choroiditis.
The availability of multimodal imaging, including fundus fluorescein angiography (FFA), spectral domain optical coherence tomography (OCT), B-scan ultrasonography (B-scan US), and indocyanine green angiography (ICGA), has increased the sensitivity for detecting early ocular inflammatory changes. ICGA has long been recognized as the gold standard for detecting subtle choroidal circulatory changes that could predict new activity or recurrence. More recently, however, the introduction of OCT angiography (OCT-A) has allowed the detection of vascular density alterations and areas of apparent flow reduction that are associated with different forms of posterior uveitis, including VKH.,,,, The appeal of OCT-A as a noninvasive imaging modality and in settings where ICGA may not be available explains its recent popularity among clinical investigators of VKH.
In this work, we report our experience with clinical and imaging evaluation of eyes belonging to Egyptian VKH patients.
| Methods|| |
This retrospective observational study included the analysis of the clinical and imaging records of patients diagnosed with VKH that presented to the uveitis services at a single private eye center during the 3-year interval between January 2018 and January 2021. The study adhered to the tenets of the Declaration of Helsinki and approval of the local ethical committee was obtained before study initiation. Data deidentification was ensured before their analysis and accordingly, informed consent was waived.
Patients aged 18 years or older who met the international revised diagnostic criteria for VKH and had undergone ocular imaging at our center were included. Both patients with acute and chronic integumentary (convalescent) presentations were included in the analysis. Convalescence was defined as the consistent absence of anterior segment (AS) inflammation, vitritis, ERD, signs of choroiditis, and papillitis on clinical examination for a duration exceeding 3 consecutive months. Patients were excluded from the analysis if they had a co-existing systemic disease known to affect the posterior segment of the eye, prior intraocular surgery (other than that for complicated cataract), secondary glaucoma or a CNV on first presentation, or when no/poor quality scans were available to verify the diagnosis and analyze the imaging findings. On diagnosis, patients were routinely referred to an immunologist who, guided by the ocular status of the patient, would tailor the systemic treatment for each patient and monitor for any adverse drug reaction.
For cases in which the inflammation or cataract did not permit a sufficiently clear fundus view for clinical judgment, B-scan US (Sonomed Escalon Vupad, Escalon Medical Corp., PA, USA) was performed to assess the posterior segment. When performed, fundus photography and FFA were captured through VISUCAM500 (Carl Zeiss Meditec AG. Goeschwitzer, Germany), while OCT and OCT-A were captured using the Avanti Widefield OCT with AngioVue (Optovue Inc., CA, USA). For OCT, radial macular scans were screened for subretinal fluid or ERD, and subfoveal choroidal thickness (SFCT) was manually measured using the built-in caliper tool in still images acquired by the choroidal mode of the machine. For OCT-A, 3 mm × 3 mm and 6 mm × 6 mm AngioRetina scans were obtained. Automated layer segmentation was performed by the machine's software, and manual adjustment of segmentation was done when needed to ensure accuracy. The term “flow deficit (FD)” was used for areas in the choriocapillaris (CC) angio-scans in which blood flow was undetectable as described in previous studies, (also defined by other groups as “flow void”, and “dark areas/spots).”, ICGA was not available at the site of this study.
The collected clinical data included age, sex, laterality, presenting symptom, stage of the disease on presentation, corrected distance visual acuity (CDVA) and intraocular pressure on presentation, clinical signs on slit-lamp biomicroscopy and fundoscopy, treatment received, follow-up duration, final clinical outcome, and ocular complications.
Statistical analysis was performed using the Statistical Package for Social Science (SPSS Version 25, IBM, Armonk, New York, United States). The Shapiro–Wilk test was used to assess departure from normality. Data were described in terms of mean and standard deviation (± SD) if normally distributed, and median with interquartile range (IQR) in case of nonnormal distribution.
| Results|| |
The final analysis included 54 eyes of 27 patients with a median (IQR) age of 30 (21–38) years, and of which 19 patients (70.37%) were female. All cases had bilateral ocular manifestations of VKH on presentation, although 4 of them (14.81%) had a unilateral complaint that was limited to the more affected eye. All patients presented during an acute uveitic state, 19 patients (70.37%) presented in an initial attack, while eight patients (29.63%) presented in the recurrent form. Concurrent extraocular manifestations were present in 13 patients (48.15%) in the form of headache (nine patients, 33.33%) and ear symptoms (seven patients, 25.93%). The main presenting symptom was a drop of vision in 24 patients (88.89%), eye pain in two patients (7.41%), and eye redness in one patient (3.7%). The median (IQR) duration from the onset of symptoms to the first presentation was 12 (7–20) days.
The major clinical examination findings on presentation are detailed in [Table 1]. Only 12 of the 54 eyes (22.22%) had a CDVA that was better than 20/40 (0.5). Seven eyes (12.96%) had AS involvement. The most common presenting sign in the posterior segment was ERD (44 eyes, 81.48%), followed by clinically detectable choroiditis (24 eyes, 44.44%). Vitritis was present in 10 eyes (18.52%) and an SGF was present in 8 eyes (14.81%).
|Table 1: Major clinical characteristics of the examined eyes on presentation (n=54)|
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On presentation, B-scan US was utilized in 4 eyes (7.41%) owing to a hazy fundus view that did not permit visualization of fundus details. The major findings were thickened choroid (4 eyes, 100%), ERD (3 eyes, 75%), and vitreous opacities (2 eyes, 50%). OCT was utilized in 48 eyes [88.89%, [Figure 1]], which revealed subretinal fluid with neurosensory detachment in 43 of them (89.58%), choroidal infiltration (irregular reflectivity of CC and elevations of Bruch's membrane) in 11 eyes (22.92%), cystoid macular edema (ME) in 7 eyes (14.58%), and subretinal fibrosis in 4 eyes (7.41%). The mean (± SD) SFCT was 331 (±106.4) um.
|Figure 1: Variable signs of presentation on OCT scans in a sample of the imaged eyes: (a) OCT B scan of a right eye during acute phase with subretinal fluid (arrows) and irregular reflectivity in the choroid with elevations of Bruch's membrane denoting choroidal infiltration (arrowheads), (b) OCT B scan of a right eye during the acute phase with a large bacillary layer detachment (asterisks) and choroidal infiltration (arrowheads), (c) OCT B scan of a left eye during acute stage with a small area of neurosensory detachment (arrow) and a thick choroid, and (d) OCT B scan of the left eye with chronic disease with an epiretinal membrane and a subfoveal scar. OCT: Optical coherence tomography|
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FFA was performed in 39 eyes [72.22%, [Figure 2]] and revealed pinpoint/punctate hyperfluorescence at the level of the RPE followed by pooling of the dye in areas of ERD in 33 eyes (84.62%), a hot disc (optic disc leakage and/or late staining) in 16 eyes (41.03%), and delayed arm-to-retina circulation in 2 eyes (5.13%). OCT-A was used for 30 eyes (55.56%), in which FD in the CC angio-scans that correlated with disease activity was detectable in 25 eyes [83.33%, [Figure 3] and [Figure 4].
|Figure 2: Fluorescein angiography appearance of two eyes during acute presentation: A left eye is shown during early phase (a) with pinpoint macular leakage, and late phase (b) with more diffuse leakage. A right eye is also shown during early phase (c) with pinpoint leakage in the posterior followed by late (d) pooling in areas of neurosensory detachment and a hot disc|
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|Figure 3: OCT-A and corresponding B-scans in the left eye of one of the patients during active and convalescent phases of the disease. Small black spots of CC flow deficit are marked with arrowheads, with marked reduction in their area from active choroiditis to convalescence. OCT: Optical coherence tomography-Angiography, CC: Choriocapillaris|
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|Figure 4: OCT-A and corresponding B-scans in the left eye of one of the patients during various stages of the disease, panels from left to right: Active disease on presentation, regression on start of treatment, convalescence, and start of recurrence. Areas of CC flow deficit are marked by arrowheads. OCT: Optical coherence tomography-Angiography, CC: Choriocapillaris|
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Twenty-four patients (88.89%) received topical corticosteroids, 24 (88.89%) received oral corticosteroids, 7 (25.93%) received intravitreal corticosteroid injection, 5 (18.52%) received immunosuppressive medication, and 3 (11.11%) received intravenous pulse steroids. Follow-up data were available for 20 patients (40 eyes, 74.07%), for which the median (IQR) duration of follow-up was 12.5 (4–29.5) months. On the latest follow-up date, CDVA improved in 34 of the 40 eyes (85%) and remained stable in 3 eyes (7.5%). In the remaining 3 eyes (7.5%) that had worsened vision on final follow-up, two belonged to a patient that presented 60 days after the onset of the first symptoms, and one belonged to a patient that presented with chronic recurrent disease in that eye and in which subretinal fibrosis had already started to develop on presentation. Complications developed in a total of 24 eyes (30%), cataract developed in 21 eyes (52.5%), glaucoma developed in 6 eyes (15%), and subretinal scarring developed in 2 eyes (5%).
| Discussion|| |
We present our experience with the clinical evaluation, different imaging findings, and outcomes in eyes of patients diagnosed with VKH. To the best of our knowledge, this is the first dedicated report on the ocular characteristics of Egyptian VKH patients. Amin et al. analyzed the different causes of uveitis in a large cohort of Egyptian patients over an interval of 2.5 years and found VKH to be the second most common identifiable cause of uveitis (11.67% of the cases). On the other hand, Hassan et al. reported a lower incidence (3.5%) of VKH in a cohort of noninfectious uveitis patients referred for rheumatological assessment.
Our findings validate the theory of the “therapeutic window” for VKH., In our cohort of patients, most cases presented and received the proper treatment during the first 3 weeks (IQR: 7–20 days) from the onset of symptoms, and 92.5% of the managed eyes that were followed up had favorable final clinical outcomes of stable or improved vision. This emphasizes the role of early evaluation on suspicion and aggressive therapeutic intervention on diagnosis in cases of VKH with ocular involvement.
There was a female predominance in our analyzed pool of patients (F:M = 2.38:1). Female predominance has been noted in other studies on VKH patients, including those conducted in other Middle Eastern countries such as Turkey and Saudi Arabia, and outside the Middle East as in India. This could be attributed to the general female bias in most systemic autoimmune diseases and may be related to hormonal alterations or to genetic factors that influence the disease occurrence. The latter possibility is supported by the fact that studies in certain geographic areas such as China and Singapore have reported no gender differences in VKH incidence within their studied samples. This highlights the importance of specifying the disease's unique demographic, clinical, and genetic patterns in each population.
The clinical characteristics of our studied eyes resemble some of those reported in previous studies. The decreased vision was the most common complaint on presentation, which was also the case in a recent large analysis of cases. ERD was the most commonly encountered clinical sign on fundus examination that was present in 81.48% of our studied eyes, and vitritis was present in 18.52% of the eyes. The incidences of ERD and vitritis in VKH patients vary significantly within literature reports according to the population and the clinical stage of presentation,,,,,, ranging from 37.5% to 95% for ERD, and from 19.4% to 76% for vitritis. The most common macular pathology encountered in our sample was ME (11.11%), which is in line with a recent large analysis of macular abnormalities in eyes with VKH in which ME represented 60.87% of detectable abnormalities. Cataract was the most common ocular complication in our studied patients, as was the case in multiple other reports.,,
The revised diagnostic criteria for VKH published in 2001 are still widely in use. The criteria necessitate the presence of bilateral choroiditis to diagnose an active (early) stage of complete, incomplete, or probable VKH. However, critique has been directed toward the criteria due to failure to include the imaging modalities that characterize stromal choroiditis. In 2018, Yang et al. attempted to provide another revision of the diagnostic criteria for early VKH that included specific findings of certain imaging modalities that had a high specificity for VKH (viz., ERD on B-scan US or OCT, choroidal thickening on EDI-OCT, and early punctate leakage and late pooling or a hyperfluorescent disc on FFA). The latter criteria, however, did not evaluate the role of OCT-A in detecting choroidal hypoperfusion.
In the recent years, OCT-A has made its way into the diagnostic toolbox of ophthalmologists in evaluating eyes with uveitis, particularly in VKH patients.,,, Areas in the CC in which FD is detected on OCT-A have been shown to correspond to areas of early choroidal hypofluorescence in ICGA, and to correlate well with disease activity and stage.,, To date, no properly structured study has evaluated the sensitivity and specificity of OCT-A for early VKH in comparison to other imaging modalities. Our setting lacked ICGA (previously considered the gold standard for diagnosing choroiditis); available FFA was able to detect the characteristic early punctate hyperfluorescence and late dye pooling in 84.62% of the studied eyes, while OCT-A could detect FD in the CC in 83.33% of the studied eyes. Another issue that faces OCT-A is the lack of consensus on the terminology used when describing findings in eyes with uveitis. A third issue is that, at least in our experience, the presence of vitritis or subretinal fluid caused shadowing artefacts in the OCT-A CC scans and affected our accurate delineation of FD areas. If those limitations are addressed, FD findings on OCT-A may soon be evaluated as an additional diagnostic criterion for early VKH and/or early detection of its recurrence.
Limitations to our study include the single-center experience and the relatively small sample size. However, being the first dedicated analysis of VKH cases in Egypt, this study is intended to serve as a cornerstone effort in characterizing the distribution, presentation, predictive factors, and treatment outcomes within the population. Another limitation is the lack of ICGA in our setting. Comparing ICGA findings to those of OCT-A would have helped evaluate the noninferiority of the latter in detecting early VKH. A final limitation is the lack of sufficient follow-up data to evaluate the role of different imaging modalities in predicting the subclinical recurrence of the disease.
| Conclusion|| |
The ocular clinical and imaging findings in a sample of Egyptian VKH patients seem to resemble those reported elsewhere in the literature, with a suggested female predominance in the population. Early detection and appropriate management during the therapeutic window stage of the acute disease are associated with a favorable visual outcome. Multimodal imaging, with the recent addition of OCT-A, provide complementary data that serve in reaching the final diagnosis, monitoring response to treatment, and detecting the recurrence of ocular VKH.
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Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]