|Year : 2013 | Volume
| Issue : 4 | Page : 134-140
Uveitis: A search for a cause
Arshee S Ahmed, Jyotirmay Biswas
Sankara Nethralaya, 18 College Road, Nungambakkam, Chennai 600 006, Tamil Nadu, India
|Date of Web Publication||20-Nov-2013|
Arshee S Ahmed
Sankara Nethralaya, 18 College Road, Nungambakkam, Chennai 600 006, Tamil Nadu
Source of Support: None, Conflict of Interest: None
This article aims to review the current literature to identify the various laboratory and investigative modalities that can be used to aid in the diagnosis of patients with uveitis. Although laboratory tests such as erythrocyte sedimentation rate, serum angiotensin-converting enzyme levels, and human leukocyte antigen typing among others have limited utility in the diagnosis of uveitis, they provide supportive evidence. Results of serological tests such as enzyme-linked immunosorbent assay have proven to be of significant importance in diagnosing diseases such as toxoplasmosis, and the use of ocular samples such as aqueous and vitreous has greatly increased the diagnostic reliability. Imaging techniques play a major role in the diagnosis of posterior uveitis. Fundus fluorescein angiography, indocyanine green angiography and lately, autofluorescence and optical coherence tomography provide information about the diagnosis of uveitis disorders and are also useful for monitoring progression, complications, and response to treatment. The use of ultrasonography and ultrasound biomicroscopy provides useful information in eyes with chronic uveitis where complications such as retinal detachment and cyclitic membranes are suspected and hazy media precludes a thorough clinical examination. Radiological investigations such as computerized tomography aid in the diagnosis and management of systemic disorders such as tuberculosis or sarcoidosis.
Keywords: angiography, autofluorescence, optical coherence, polymerase chain reaction, uveitis
|How to cite this article:|
Ahmed AS, Biswas J. Uveitis: A search for a cause. Taiwan J Ophthalmol 2013;3:134-40
“Diagnosis is not the end, but the beginning of practice.”
Martin H. Fischer
Rarely has a field of medicine been more challenging than the field of intraocular inflammation. The study of uveitic entities presents great challenges to the treating ophthalmologists because the list of differential diagnosis ever grows to encompass a range of diseases from infectious to immunological to malignant. To the trained eye, though, a methodical system of clinical examination and a pick of the most useful investigative modalities would lead to adefinitive diagnosis in a majority of cases. In this article, we present a fresh look at the plethora of investigations at our disposal and the usefulness of these in arriving at a diagnosis.
Uveitis has been classified into various subdivisions according to the Standardization of Uveitis Nomenclature and International Uveitis Study Group classification. It could be anterior, intermediate, posterior, or a panuveitis depending on the primary site of inflammation. It could also be classified based on etiology as infectious, noninfectious, or a masquerade. The list of differentials under each category is mind-boggling and many times similar clinical pictures can pose diagnostic challenges. Therefore, here lies the usefulness of investigative modalities to narrow down the search for a cause. The role of these tests lies in obtaining diagnostic and prognostic information and in taking a therapeutic direction. A logical sequence of events would be to compare clinical characteristic with known uveitic entities and shortlist etiological possibilities. Then first order relevant laboratory investigations and order extensive investigations if refractory to treatment.
Simple tests such as a complete blood count, erythrocyte sedimentation rate (ESR), and C-reactive protein may give information about the nature of the underlying disease. The ESR is a simple and inexpensive laboratory test. It is commonly used to assess the acute-phase response. For example, a raised ESR is seen in conditions such as tuberculosis, syphilis, sarcoidosis, and collagen vascular disorders.
Levels of serum angiotensin-converting enzyme (ACE) have an important prognostic role to play in the diagnosis and management of sarcoidosis. Elevated levels often favor the disease, and response to treatment can be assessed by decreasing levels of ACE. However, patients on systemic steroids and ACE inhibitors may have false-negative values. This test is indicated in all patients with granulomatous uveitis, intermediate uveitis, vasculitis, and those presenting with choroidal nodules. Serum lysozyme is much less specific for sarcoidosis than serum ACE, and therefore, its diagnostic value may be limited.
Disorders of the immune system have been implicated in the pathogenesis of noninfectious uveitis. The most frequently performed serological tests for uveitis are human leukocyte antigen (HLA) HLA-B27 and HLA-B51, rheumatic arthritis antibody, anti-nuclear antibody (ANA), enzyme-linked immunosorbent assay (ELISA), and antineutrophilic cytoplasmic antibody (ANCA).
Several HLA haplotypes are associated with ocular or systemic noninfectious posterior uveitis. HLA-B27-associated uveitis is the most common identifiable cause for anterior uveitis. It is associated with a typical, unilateral acute anterior uveitis seen in males in the age group of 30–40 years of age, with a nongranulomatous anterior chamber reaction. It accounts for between 18% and 32% of all anterior uveitis cases in Western countries and between 6% and 13% of all anterior uveitis cases in Asia. The presence of HLA-B27 is also associated with other rheumatologic diseases such as ankylosing spondylitis.
Another commonly performed HLA test is HLA-B51, for diagnosing Behçet’s disease. It is considered to be a marker for more severe disease and may increase the risk for development of complications such as uveitis, erythema nodosum, and the fullblown syndrome.,
Rheumatoid factor is most often used for the diagnosis of rheumatoid arthritis although it can be positive in various other conditions such as systemic lupus erythematosus (SLE), sclero-derma, and dermatomyositis. It is indicated in the work-up of patients who present with sclerouveitis.
Antinuclear antibodies are positive in up to 95% patients with SLE and scleroderma. Immunofluorescence is commonly used to detect antinuclear antibodies and is considered to be the gold standard. ANA testing has 95% sensitivity for SLE. It carries low specificity and can be positive in various diseases.
ANCA should be ordered in suspected cases of Wegener’s granulomatosis (WG). Sequential measurements of titers of cyto-plasmic ANCA (c-ANCA) may be useful to indicate the clinical course of patients with WG. Changes in titer of ≥2 serial dilutions are considered significant. Positivity for c-ANCA is a sensitive (88%) marker of active WG.
ELISA is commonly performed to look for the presence of antigens or specific antibodies in the sera of patients. It is commonly performed for toxoplasmosis, human immunodeficiency virus (HIV), and toxocariasis [Figure 1].
|Figure 1: A 42-year-old male patient with toxoplasmosis in the left eye. Enzyme-linked immunosorbent assay of aqueous sample was positive for Toxoplasma.|
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ELISA for toxoplasmosis carries up to 98% sensitivity and 50% specificity. Toxoplasmosis serology, contrary to the popular belief, is useful to confirm active toxoplasmic retinochoroiditis; it is easy to perform, inexpensive, and supports clinical diagnosis in up to 96% of cases, not only by showing positivity, but also by showing a significant elevation of titers. In atypical cases, serology is not only useful but also essential. Determination of intraocular antibody synthesis may be useful in atypical cases using polymerase chain reaction (PCR) and the Goldmann–Witmer coefficient, based on a correlation between titers of anti-Toxoplasma gondii antibodies in the aqueous humor and the serum, versus the globulin titers in the same fluids., PCR of the aqueous or vitreous humor can be used in uncertain cases to establish a diagnosis of toxoplasmosis.
Similarly, ELISA with Toxocara excretory-secretory antigen has been shown to be highly specific for Toxocara infection.
Analysis of intraocular fluids has gained wide popularity for the diagnosis of both anterior and posterior uveitic entities, more so for posterior uveitis that poses diagnostic dilemmas. The most common causes of infectious uveitis in immunocompetent individuals are herpes simplex virus types 1 and 2, varicella–zoster virus, and the parasite T. gondii. PCR amplifies the deoxyribonucleic acid (DNA) or ribonucleic acid of pathogens, making them easier to detect, especially when present in small quantities. PCR is superior in terms of sensitivity, specificity, and rapidity of diagnosis. Analysis of a small sample of aqueous humor may be adequate to confirm a clinically suspected intraocular infection, in particular in the context of suspected viral retinitis. Anterior chamber paracentesis has the advantage of being quick, relatively straightforward to perform, and can be carried out in the outpatient setting. In cases of posterior uveitis, vitreous sampling is necessary. This can be obtained by either a vitreous cutter or by using a 23-G needle. Formal pars plana vitrectomy requires an operation and needs to be carried out by a skilled ophthalmic surgeon. This allows up to 2 mL of undiluted vitreous to be sampled and sent for analysis. The three main indications for sampling the vitreous are suspected intraocular infection, suspected intraocular lymphoma, and an atypical response to therapy during the treatment of presumed autoimmune intraocular inflammation.
Various study groups have characterized the relative merits of aqueous PCR and intraocular antibody testing (Goldmann–Witmer coefficient) in determining the diagnosis of immunocompromised and immunocompetent patients with uveitis. They find that the two approaches are complementary; for example, in the immu-nocompromised population, PCR is superior for detecting viral infection, whereas intraocular antibody assays are superior for the diagnosis of toxoplasmosis.,, PCR for viral uveitis is indicated in atypical cases and testing is likely to be positive, including retinal vascular inflammation, extensive retinitis, optic nerve involvement, and immunocompromised state. It carries a sensitivity of 80.9% and a specificity of 97.4%.
False-positive results are another marked pitfall to the routine use of PCR as the possibility of laboratory contamination or detection of latent DNA or DNA of normal flora becomes limiting.
PCR for intraocular tuberculosis is extremely useful and various ocular tissues can be used for testing including aqueous humor, vitreous humor, subretinal fluid, and tissue obtained by chorior-etinal biopsy. Both real-time and nested PCR have been used in the diagnosis [Figure 2] and [Figure 3].,,,
|Figure 2: A 48-year-old male presented with decreased vision in both eyes after a bout of febrile illness. Fundus findings included multiple exudates and hemorrhages. Real-time polymerase chain reaction from aqueous tested positive for Chikungunya virus.|
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|Figure 3: A 34-year-old male patient with serpiginous-like choroiditis. In addition, the quantitation report of the real-time polymerase chain reaction on aqueous sample revealed Mycobacterium tuberculosis DNA.|
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Skin testing is commonly performed for diseases such as tuberculosis. The most commonly performed of these tests is the Mantoux test, which involves intradermal injection of purified protein derivative and assessing the resulting induration. It is based on the hypersensitive reaction toward the mycobacterial antigens. Its disadvantages are that it is not specific for Mycobacterium tuberculosis and does not distinguish latent infection from the disease. It may be positive with cases involving Bacillus Calmette–Guerin (BCG) vaccination/exposure to atypical mycobacteria and may be negative in immunosuppressed states/children/extrap-ulmonary or miliary tuberculosis. Its value is now becoming limited in endemic countries such as India because 30–69% of healthy adults would test positive and it could be negative or weakly positive in up to 33% of patients with tuberculosis.,
Interferon-gamma release assays are tests that measure the interferon-γ release after in vitro stimulation of patients’ lymphocytes with M. tuberculosis-specific antigens. These are more specific markers of M. tuberculosis infection/previous exposure. The advantages are that it is not influenced by BCG vaccination or exposure to atypical mycobacteria and not as subject to biases and errors of placement and reading as the tuberculin skin-sensitivity tests. Disadvantages are the higher cost and limited availability. It is possibly the most sensitive to detect latent infection than tuberculin skin tests but does not distinguish it from active disease. It may also be negative or indeterminate in immunosuppressed states.,,,
Fundus fluorescein angiography (FFA) is invaluable in patients with uveitis as it demonstrates changes secondary to intraocular inflammation and helps in monitoring the response to therapy [Figure 4]. It aids in the diagnosis of cystoid macular edema, which is one of the most common causes of visual morbidity in patients suffering from uveitis. Classically, it appears as a flower-petal-shaped leakage of dye from the macular capillaries. Yannuzzi et al classified macular edema into five grades depending on the extent of hyperfluorescence noted.
|Figure 4: Fundus photo and fluorescein angiogram reveal uveitic macular edema in a patient with pars planitis.|
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FFA is useful in demonstrating the extent of retinal vasculitis by showing leakage of dye and staining of the walls of major retinal vessels in the areas of localized inflammation., Conditions such as intermediate uveitis, sarcoidosis, and Behcet’s disease are frequently associated with vasculitis. Neovascularization of the disc and elsewhere is very well demonstrated by FFA as it shows extensive dye leakage from the fragile vessels. In conditions such as Eales disease, extensive areas of capillary nonperfusion also may be made out.
FFA is characteristic in patients with Vogt–Koyanagi–Harada’s (VKH) syndrome with exudative retinal detachment, showing multiple, pin-head leaks at the level of the retinal pigment epithelium (RPE) and the presence of subretinal fluid. Disc leakage is considered to be an important sign of activity. Exudative retinal detachments occurring at the posterior pole are also seen in posterior scleritis.
FFA findings in the so-called white dot syndromes are characteristic as they show early hypofluorescence followed by late hyperfluorescence seen in acute posterior multifocal placoid pigment epitheliopathy, birdshot chorioretinopathy, and serpigi-nous choroiditis.,,,, However, lesions in multiple evanescent white dot syndrome show early-phase FA, demonstrating punctate hyperfluorescence corresponding to the white dots seen clinically, which persist into the late phase. There is also leakage of the optic disc in most cases.
Choroidal neovascularization (CNV) can complicate many of the uveitic diseases, and is most commonly seen in multifocal choroi-ditis, punctuate inner choroidopathy, serpiginous choroiditis, and presumed ocular histoplasmosis syndrome [Figure 5] and [Figure 6]. It can also occur in toxoplasmic retinochoroiditis, VKH syndrome, bird-shot chorioretinopathy, and in various other entities.
|Figure 5: Peripapillary choroidal neovascular membrane in a patient with healed toxoplasmosis.|
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|Figure 6: Active serpiginous choroiditis with typical fundus autofluorescence showing hyperfluorescent borders suggestive of activity.|
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Discrepant FFA and optical coherence tomography (OCT) findings were noted in 46% of uveitic eyes in one study, predominantly occurring in eyes with mild macular edema. Although the FFA+/OCT+ consistency was noted frequently in active uveitis, the FFA-/ OCT+ discrepancy was common in eyes with inactive uveitis. These results show that FFA and OCT are complementary investigations, each revealing different aspects of the pathophysiological features of uveitic macular edema, and this may influence the therapeutic decisions.
Fundus autofluorescence (FAF) is a new technique that allows topographic mapping of lipofuscin distribution in the retinal pigment epithelium cell monolayer as well as of other fluorophores that may occur with disease in the outer retina and the sub-neurosensory space. FAF imaging gives information above and beyond that obtained by conventional imaging methods, such as fundus photography, FA, and OCT. Its clinical value coupled with its simple, efficient, and noninvasive nature is increasingly appreci-ated. In patients with serpiginous choroiditis, increased auto-fluorescence (hyperfluorescence) may be seen in acute phases. During the resolution stages of inflammation, the pigment in the lesion becomes slate gray. With this change comes a decrease in the amount of visible autofluorescence. Regressed or inactive lesions show hyperfluorescence. Slate or neutral gray-black areas frequently have a complete absence of autofluorescence. Secondary CNV often is easy to recognize by FAF imaging because the surrounding hyperplastic RPE is hyperautofluorescent and neatly outlines the neovascularization. This hyperautofluorescence persists for years after the CNV has formed. After treatment, CNV may contract and leave a zone of absent RPE in a manner similar to that of inflammatory lesions.
Indocyanine green angiography (ICGA) was first described in 1973 and since then has been a better imaging modality for viewing the choroidal vasculature than FA. The major application of ICGA is in disorders involving the choriocapillaris and the choroid. ICG is more protein bound, and therefore, leakage from the fenestrations of the choriocapillaris is reduced, enabling better visualization of the choroidal circulation. Most information is obtained from the late phases of the study. Recently, these disorders have been classified into two groups based on findings revealed by ICGA. Type 1 is the inflammatory choriocapillaropathies and appears as hypo-fluorescence in both the mid and late phases of the ICGA study. Examples of this are the various white dot syndromes [Figure 7]. Type 2 represents stromal inflammatory vasculopathies and is characterized by late leakage of ICG dye from inflamed choroidal vessels. Sarcoidosis, tuberculosis, VKH disease, sympathetic ophthalmia, birdshot chorioretinopathy, Behcet’s disease, and posterior scleritis are examples of stromal involvement.
|Figure 7: Fundus photograph, fluorescein angiography, and indocyanine green angiography (ICGA) in a patient with multiple evanescent white dot syndrome. The ICGA highlights the multiple hypofluorescent spots that are not picked up on fundus fluorescein angiography.|
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The ICGA study is helpful in differentiating an inactive chorior-etinal scar from active CNV. Scars appear hypofluorescent throughout the angiogram, whereas the CNV may present as a hot spot of hyperfluorescence in the midphase of the study, with late leakage.
OCT is a noninvasive, noncontact tool, which uses the principle of low coherence interferometry to take axial and transverse scans of the retina using a light source [Figure 8]. It is very useful in the diagnosis and follow-up of macular disorders such as cystoid macular edema due to uveitis, epiretinal membranes, vitre-omacular traction, and even choroidal neovascular membranes. Various studies have studied the role of OCT in uveitic eyes and have tried to assess the correlation between visual acuity and OCT findings. Some suggest a strong correlation, whereas others suggest weak correlation. One study described three patterns of macular edema in patients with uveitis: diffuse macular edema, cystoid macular edema, and retinal detachment. It is especially useful for the diagnosis of macular detachment, which is difficult to pick up on FFA. Recently, newer techniques such as enhanced-depth imaging–OCT have allowed us to measure choroidal thickness, which may serve as a marker for degree of choroidal inflammation in acute VKH disease.
|Figure 8: Optical coherence tomography in a patient with chronic pars planitis showing typical cystic spaces suggestive of cystoid macular edema.|
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Ultrasonography (B scan) is useful in demonstrating vitreous opacities, choroidal thickening, retinal detachment, or cyclitic membrane formation, particularly if media opacities preclude a view of the posterior segment. This may be the result of the presence of corneal opacification, anterior chamber hyphema or hypopyon, pupillary miosis, cataract, lenticular membranes, or vitreous hemorrhage or inflammation [Figure 9] and [Figure 10].
|Figure 9: Ultrasonogram of a patient showing a large subretinal abscess.|
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|Figure 10: Diffuse choroidal thickening noted in a patient with Vogt–Koyanagi–Harada's syndrome.|
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B-scan ultrasound is useful in quantifying scleral thickness. Highly reflective echoes with thickening of the uvea and sclera are usually present. Scleral edema associated with fluid within Tenon’s space results in an echolucent region just posterior to the sclera, the so-called T sign. This is considered virtually diagnostic of posterior scleritis.,
Ultrasound biomicroscopy (UBM) uses high-frequency ultrasound waves (40–60 MHz) to allow high-resolution examination of the anterior segment, ciliary body, and pars plana region. In patients with intermediate uveitis, UBM allows the documentation of pars plana exudates and membranes in eyes with hazy media or small pupil. It is also useful for assessing the severity and extent of involvement in patients with peripheral toxocariasis. In eyes with chronic hypotony, UBM gives clues as to the presence of chronic ciliary membranes resulting in ciliary body shutdown.,,
Radiological investigations such as high-resolution computerized tomography (HRCT) are useful for suspected cases of uveitis secondary to systemic diseases such as tuberculosis and sarcoid-osis. According to one study, 81% of uveitis patients referred for chest HRCT demonstrated signs suggestive of tuberculosis, 8.6% patients showed signs suggestive of sarcoidosis, and 10.3% patients showed normal chest HRCT. Chest HRCT was found to be a useful tool in the diagnosis of granulomatous uveitis, especially tuberculosis-associated uveitis, and can aid in therapeutic decisions.
In conclusion, a modern approach to uveitic disorders is to look for specific uveitic entities rather than ordering a battery of tests. For example, in a patient with recurrent attacks of non-granulomatous anterior uveitis, it would be appropriate to order rheumatoid factor, antinuclear antibodies, and ESR. In addition, based on medical history, one could look for HLA-B27, venereal disease research laboratory (VDRL), Treponema pallidum hemag-glutination assay (TPHA), and a chest X-ray along with the Mantoux test to rule out tuberculosis. Similarly for a granulomatous anterior uveitis, tests for sarcoidosis should also be advised. Likewise, for intermediate uveitis, tests for tuberculosis, sarcoidosis, and even multiple sclerosis may be needed along with ancillary tests such as OCT to track structural changes (e.g., cystoid macular edema), which are a major cause of drop in visual acuity in these patients. In patients suffering from posterior uveitis, the commonly performed tests are ELISA for Toxoplasma, Mantoux test, serum ACE and lysozyme levels, VDRL, and TPHA. Tests for HIV should be included whenever there is a high clinical suspicion of the disease. Ancillary tests should include FFA, ICG, OCT, and ultrasonography as indicated. Established entities such as Behcet’s disease, sympathetic ophthalmia, or VKH syndrome require a clinical diagnosis and no specific diagnostic test is needed. To conclude, arriving at a diagnosis is possible in a majority of the patients with uveitis using a targeted approach. Detailed initial examination and keeping in mind the various differentials can lead to selection of appropriate laboratory and ancillary tests.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
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