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Sarcoidosis: experience in a Mexican ophthalmological clinic

BMC Ophthalmology volume 23, Article number: 330 (2023) Cite this article

Abstract

Background

Sarcoidosis is an inflammatory disorder in which patients frequently develop ocular manifestations that precede systemic involvement, sometimes it even presents as an ocular isolated form of the disease. The purpose of this study is to report the ocular and systemic manifestations of sarcoidosis in a series of Mexican patients, as there is a low incidence of the disease in this population.

Methods

A retrospective case series of patients with positive classification criteria for sarcoidosis who attended Asociacion Para Evitar la Ceguera en Mexico, IAP between 2011 and 2022. Descriptive statistics were used to report the clinical, laboratory, and imaging findings and treatment. Numerical results were presented using median values and first and third quartiles for distribution.

Results

Fourteen patients were included in this study, 10 of them had definite ocular sarcoidosis (biopsy-proven), 4 had presumed ocular sarcoidosis. The median age of onset was 52 (34; 67), with a predominance of female patients (71.4%). Ten patients (71.4%) debuted with ocular manifestations. The most common forms of ocular involvement were bilateral anterior uveitis (50%) and panuveitis (28.6%). Median follow-up was 24 (13–49) months.

Conclusions

Sarcoidosis is a rare, underdiagnosed condition in Mexico and ocular involvement can be an early manifestation of the disease. Ophthalmologists should be alert to the signs of ocular sarcoidosis and collaborate with a multidisciplinary team to screen for systemic involvement if suspicion is high.

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Background

Sarcoidosis is an inflammatory disorder of unknown cause, characterized by systemic inflammation and the formation of noncaseating epithelioid cell granulomas, which can affect practically every organ [1]. It’s incidence is estimated to be 5.9/100,000 for men and 6.3/100,000 for women in United States, [2] and it is a relatively common cause of uveitis in European patients [3].

Despite this, sarcoidosis in Latin America is rare, and the information on its prevalence, risk, and morbidity in Hispanic patients is limited [4,5,6,7]. There are only 28 published cases of sarcoidosis in Mexico and only 5 which report ocular manifestations (Table 1) [4, 8,9,10,11,12,13,14].

Table 1 Sarcoidosis in Mexico 1991–2022
Full size table

There is a wide spectrum of systemic manifestations of sarcoidosis that encompass many specialties in medicine. Lungs are the most affected organ in the disease (more than 90% of all cases) [15]. Although these manifestations are mainly non-specific of sarcoidosis, such as dyspnea, cough, and chest pain, lung imaging studies help identify specific signs that support the diagnosis. The two main imaging findings in pulmonary sarcoidosis are bilateral hilar lymphadenopathy (BHL) and perilymphatic pulmonary nodules [16].

The second most affected organ in patients with sarcoidosis is the eye. Up to 30–50% of patients with systemic sarcoidosis will show eye involvement, or it can only be confined to the eye. The two main ocular manifestations are keratoconjunctivitis sicca and uveitis. Regarding ocular inflammation, anterior uveitis and panuveitis are the most common form of presentation, although the disease can affect any section of the eye [17,18,19,20].

Ocular manifestations are often bilateral. These include orbital and adnexal non-specific manifestations, such as keratoconjunctivitis sicca (dry eye), dacryocystitis, conjunctival granulomas, and less commonly diffuse orbital inflammation, ocular nerve palsy, and scleral granulomas [22].

Specific ocular manifestations support clinical diagnosis and help differentiate sarcoid uveitis from other types of inflammation. These are often accompanied by a sudden onset of pain or loss of visual acuity and include anterior segment signs such as mutton fat keratic precipitates (granulomatous uveitis) iris nodules either at the pupillary margin (Koeppe) or in the stroma (Busacca), Berlin nodules (trabecular meshwork nodules) and anterior tent-shaped synechiae at the iridocorneal angle. There are also intermediate and posterior inflammatory manifestations like snowbanking and snowball vitreous opacities, candle wax vascular shedding (retinal periphlebitis), microaneurysms, and optic disc nodules (granulomas). These manifestations guide the diagnosis of ocular sarcoidosis [1, 19, 21, 23].

Other manifestations include specific syndromes that have ocular and systemic manifestations, which help diagnose sarcoidosis without the need for a confirmatory biopsy, and include Heerfordt–Waldenström syndrome (uveoparotid fever), a combination of facial palsy, parotid gland enlargement, uveitis, and low/grade fever, and Löfgren syndrome, a combination of fever, BHL, erythema nodosum with migratory arthritis including or without ankle [22].

The aim of this study is to report the ocular manifestations, systemic involvement, management, and outcome of sarcoidosis in a Mexican ophthalmology clinic.

Methods

Medical charts, and records from patients who arrived at the Inflammatory Eye Disease Clinic from 2011 to 2022, in Association Para Evitar la Ceguera en México were retrieved and classified using the revised International Criteria for the Diagnosis of Ocular Sarcoidosis (IWOS) and the Standardization of Uveitis Nomenclature (SUN) classification criteria for ocular sarcoidosis [2, 21, 24]. Patients classified as “presumed sarcoidosis” and “definite sarcoidosis” were included. Initial and final Snellen best-corrected visual acuity (BCVA) were documented.

Furthermore, the clinical evolution of each patient was classified using the SUN nomenclature of clinical status which includes inactive (grade 0 cells on anterior chamber), worsening activity (two-step increase in inflammation of anterior chamber cells or vitreous haze, or increase from 3 + to 4+), improved activity (two-step decrease in the level of inflammation of anterior chamber cells or vitreous haze, or decrease to grade 0), remission (inactive disease for > 3 months after discontinuation of treatment) [24].

A rheumatologist performed a systemic evaluation with laboratory and imaging studies. Systemic involvement findings were collected using the updated World Association of Sarcoidosis and Other Granulomatous Disorders (WASOG) tool [1]. Diagnosis was based on the guidelines of the American [25] and British [26] Thoracic Societies. Classic syndromes such as Löfgren (a triad of fever, erythema nodosum, bilateral hilar lymphadenopathy, and associated migratory arthritis, including ankle) and Heerfordt-Waldenström (parotid gland enlargement, facial palsy, anterior uveitis, and fever) were also included.

Laboratory studies included angiotensin-converting enzyme (ACE), which is an enzyme produced by epithelioid cells derived from activated macrophages (characteristic of sarcoidosis) and lysozyme (LYS) is an enzyme produced by giant epithelioid cells, that reflects the presence of granulomas. Both were considered high when they exceeded > 120% of the laboratory reference value, blood serum calcium, and lymphocyte count values were collected retrospectively when available. Hypercalcemia was defined as serum calcium > 10.2 mequ/L and lymphopenia as < 1000 lymphocytes. Also, infectious diseases were ruled out, including syphilis, with a negative venereal disease research laboratory (VDRL) test and FTA-ABS, and tuberculosis with the tuberculin test (PPD) and/or IGRA test [27]. If a patient presented with a positive PPD test for tuberculosis, a negative IGRA test and a positive biopsy for sarcoidosis could still discard tuberculosis [2].

Pulmonary involvement was defined as the presence of micronodules, atelectasis, hilar lymphadenopathies, or parenchymal changes without predisposing factors. The amount of involvement was categorized using the Scadding test for chest X-rays [16]. Chest computed tomography (CT) was also included when available [28].

Confirmation was achieved with the presence of non-caseating granulomas, Schawman, or asteroid bodies in a tissue biopsy or a classic specific form of sarcoidosis, such as Heerfordt´s or Lofgren´s syndromes [2, 21].

Results were analyzed using the IBM Statistical Package for the Social Sciences (SPSS) 25.0. Descriptive statistics were used to report the clinical, laboratory, and imaging data. Numerical results were presented using median values and first and third quartiles for distribution.

The study was approved by the Institutional Review Board (IRB) of our hospital and adhered to the tenets of the Declaration of Helsinki.

Results

Fourteen patients with a clinical and/or histological diagnosis of sarcoidosis were identified. The median age was 52 years (27; 67), and 71.4% (n = 10) were female. The median follow-up was 24 (13–49) months. Two patients had tattoos and one had a history of smoking. Ten (71.4%) patients were defined as a biopsy-proven definite diagnosis of ocular sarcoidosis (Table 2), and 4 (28.6%) as a presumed diagnosis by bilateral hilar lymphadenopathy (BHL) and classical ocular signs.

Table 2 Characteristics of patients with definite ocular sarcoidosis
Full size table

All fourteen patients fulfilled the SUN classification criteria for ocular sarcoidosis.(Tables 2 and 3). The most common ocular presentations were anterior uveitis (n = 7, 50%), and panuveitis (n = 4, 28.6%). Uveitis was granulomatous in 4 (28.6%) patients. Anterior chamber cells were detected in 12 patients (85.6%). Adnexal manifestations included dacryoadenitis (n = 2, 14.3%), and conjunctival granuloma (n = 1, 7.1%). Only two patients (14.3%) presented clinically relevant keratoconjunctivitis sicca. Six (42.8%) of the biopsy confirmed patients debuted with ocular manifestations, all developed systemic manifestations of sarcoidosis during follow-up. (Table 3).

Table 3 Patient ocular and systemic manifestations
Full size table

All patients had systemic involvement; most commonly general symptoms (n = 8, 57.1%), and pulmonary manifestations (n = 7, 50%) (Tables 2 and 3).

ACE serum levels were available in 10 (71.1%) patients, 6 (60%) had increased levels, with a median concentration of 70.5 (38.6; 89) UI/l. Lysozyme was available in 8 patients (57.1%), showing high levels in 5 cases (62.5%) with a median of 3.81 (5.6; 24) mg/L. PPD was available for 13 patients; one had a positive result, so tuberculosis was discarded by clinical picture, negative IGRA, and a positive skin lesion biopsy for sarcoidosis [2]. Patient biopsies were collected from the skin (n = 5, 55%), lacrimal glands (n = 2, 22%), bronchi (n = 2, 22%), and vitreous body (n = 1, 11%).

A chest X-ray was obtained in 9 patients (64.3%) and a CT scan for 13 patients (92.8%). Both studies were available in 8 patients. (Table 3)

All patients received treatment. (Table 4) Topical 1% prednisolone (64.28%) and oral prednisone (92.8%) were the most common initial treatment. Immunomodulators were prescribed to 12 (85.7%) patients, including azathioprine (n = 6, 42.8%), methotrexate (n = 6, 42.8%), and adalimumab (n = 1, 7.1%); these allowed early removal of corticosteroid therapy in 6 patients (42.8%) with adequate response. These medications were started due to ocular manifestations in eight (57.1%) patients. On their last visit, 10 (71.42%) patients had remission of both systemic and ocular inflammation, 4 (28.6%) patients remained with ocular inflammation, and one as worsening activity of uveitis. Treatment for patients with persistent inflammation consisted of prednisone (n = 4, 100%), azathioprine (n = 2, 50%), methotrexate (n = 3, 75%), and topical steroids (n = 2, 50%).

Table 4 Patients treatment, visual outcome, and ocular complications
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Nine (64.28%) patients with a definite diagnosis had long-term ocular complications (Table 4). At the end of the follow-up, eleven eyes (39.28%) had a visual outcome worse than 20/50, and seventeen eyes (60.7%) had an outcome better than 20/50 (logMAR 0.39).

Discussion

This study describes the clinical characteristics of 14 patients diagnosed with sarcoidosis. This is the largest series of Mexican subjects with ocular sarcoidosis to date, as previous Mexican studies have only reported 5 cases of patients with ocular disease [4, 8,9,10,11,12,13,14]. Our institution is a reference center for ocular inflammatory diseases in our country, which allows us to analyze some of the less common diseases in our population, such as sarcoidosis.

In this sample of patients, we found a greater proportion of female patients with either definite (70%) or presumed (75%) sarcoidosis, which is similar to previous international reports (Table 5). Our patients’ most common extraocular manifestations are similar to the previous Mexican case series of systemic sarcoidosis [4].

Table 5 Ocular Sarcoidosis around the world
Full size table

Anterior uveitis was the most common anatomical location, which contrasts with previous international reports of ocular sarcoidosis [19, 20, 29, 30]. (Table 5). Even though keratoconjunctivitis sicca is one of the most common classical presentations in sarcoidosis, only two patients had clinically relevant findings supporting this condition.

All our patients had systemic involvement and activity of the disease compared to previous reports with ranges from 36.6 to 62.6% [17, 19] probably due to the sample size and that our patients had ocular manifestations that led them to seek medical attention. The main clinical signs of systemic involvement were like international reports, involving the skin, musculoskeletal and pulmonary [17, 19].

There are plenty of studies that show an ample group of ocular manifestations as the leading manifestation to diagnose sarcoidosis, ranging from 63 to 100% [19, 20, 30]. Our patients are within that range, finding that 71.4% of patients had ocular activity as the first detectable change in sarcoidosis [31, 32]. For this reason, ophthalmologists should pay attention to early signs of ocular sarcoidosis, as prompt treatment may avoid systemic activity.

Other aspects of patient history, such as tattoos, are associated with cutaneous sarcoidosis, systemic sarcoidosis with uveitis, and isolated sarcoid uveitis [33]. In our study, two patients had permanent tattoos and did not have a reactivation or disease worsening during the follow-up.

The diagnosis of sarcoidosis is often confused with tuberculosis in endemic countries, [27] and Mexico is among the top five countries with the most cases of tuberculosis in America [34]. There is a diagnostic challenge differentiating the uveitic picture caused by both diseases, and an erroneous diagnosis of tuberculosis could be the reason for the low prevalence of sarcoidosis in Mexico.

We can observe in this study that ocular sarcoidosis can precede systemic manifestations. We must consider sarcoidosis as a differential diagnosis in patients with inflammatory eye diseases, start the diagnostic approach as an ophthalmologist and rely on a multidisciplinary group for proper systemic diagnosis and treatment.

Some of the strengths of the present study are that this is the largest group of sarcoidosis reported in the Mexican population, which can help us identify the disease characteristics, in a tertiary ophthalmology clinic. Furthermore, almost every clinical presentation of sarcoidosis was present in our series; including classic syndromes like Löfgren and Heerfordt, which are rarely mentioned even in international studies (Table 5) [2, 21].

Conclusions

Ocular manifestations, although diverse, can be crucial in the suspicion and diagnosis of systemic sarcoidosis. In our experience, every patient that starts as an isolated form of ocular inflammation later resulted in systemic sarcoidosis. Therefore, ophthalmologists should be attentive to the manifestations of ocular sarcoidosis, and screen for systemic involvement, along with a multidisciplinary team, when suspicion is high.

Data Availability

The data that support the findings of this study are available from the corresponding author, LECR, upon reasonable request.

Abbreviations

IWOS:

International Criteria for the Diagnosis of Ocular Sarcoidosis

SUN:

Standardization of Uveitis Nomenclature

WASOG:

World Association of Sarcoidosis and Other Granulomatous Disorders

ACE:

Angiotensin Converting Enzyme

LYS:

Lysozyme

VDRL:

Venereal disease research laboratory

PPD:

Tuberculin test

BHL:

Bilateral Hilar Lymphadenopathy

SCAD:

Scadding score on chest X-ray

CT:

Computed Tomography

PDN:

Prednisone

MTX:

Methotrexate

AZA:

Azathioprine

HCQ:

Hydroxicloroquine

MMF:

Mycophenolate mofetil

ADA:

Adalimumab

Bx:

Biopsy

Txt:

Treatment

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Authors and Affiliations

  1. Asociacion Para Evitar la Ceguera en México Hospital Dr. Luis Sánchez Bulnes, Mexico City, Mexico

    Javier Alejandro Salazar-Rodríguez

  2. Inflammatory Eye Disease Clinic, Asociacion para Evitar la Ceguera en México, I. A. P, México City, Mexico

    Diana Sarmiento-Forero, Claudia Hubbe-Tena & Luz-Elena Concha-del-Rio

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  1. Javier Alejandro Salazar-Rodríguez
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Contributions

ASR collected and analyzed the patient data and was a major contributor to writing the manuscript. DSF Revised and was a major contributor to writing the manuscript. CHT Revised and was a major contributor to writing the manuscript. LECR Drafted the work, revised and was a major contributor to writing the manuscript. All authors read and approved the final manuscript.

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Correspondence to Luz-Elena Concha-del-Rio.

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All procedures in this study were in accordance with the ethical standards of the hospital and with the 1964 Helsinki Declaration and its later amendments. This study was approved by the institutional ethics committee “Comité de Etica de la Asociación Para Evitar la Ceguera en Mexico APEC”. Informed consent for participation in this study was obtained from all patients.

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Salazar-Rodríguez, J.A., Sarmiento-Forero, D., Hubbe-Tena, C. et al. Sarcoidosis: experience in a Mexican ophthalmological clinic. BMC Ophthalmol 23, 330 (2023). https://doi.org/10.1186/s12886-023-03081-2

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