Ocular Immunology and Inflammation
ISSN: 0927-3948 (Print) 1744-5078 (Online) Journal homepage: http://www.tandfonline.com/loi/ioii20
Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center Farzan Kianersi MD, Zahra Mohammadi MD, Heshmatollah Ghanbari MD, Seyed Mohammad Ghoreyshi MD, Hadi Karimzadeh MD & Masoud Soheilian MD To cite this article: Farzan Kianersi MD, Zahra Mohammadi MD, Heshmatollah Ghanbari MD, Seyed Mohammad Ghoreyshi MD, Hadi Karimzadeh MD & Masoud Soheilian MD (2015) Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center, Ocular Immunology and Inflammation, 23:4, 278-282, DOI: 10.3109/09273948.2014.902474 To link to this article: http://dx.doi.org/10.3109/09273948.2014.902474
Published online: 16 Apr 2014.
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Date: 21 September 2015, At: 23:38
Ocular Immunology & Inflammation, 2015; 23(4): 278–282 Copyright ! Taylor & Francis Group, LLC ISSN: 0927-3948 print / 1744-5078 online DOI: 10.3109/09273948.2014.902474
ORIGINAL ARTICLE
Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center Farzan Kianersi, MD1, Zahra Mohammadi, MD2, Heshmatollah Ghanbari, Seyed Mohammad Ghoreyshi, MD1,3, Hadi Karimzadeh, MD3, and Masoud Soheilian, MD4
MD
1
,
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1
Department of Ophthalmology, School of Medicine, Isfahan University of Medical Science, Isfahan, Iran, 2 Isfahan Eye Research Center, Feiz Eye Hospital, Isfahan University of Medical Sciences, Isfahan, Iran, 3 Department of Rheumatology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran, and 4Department of Ophthalmology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
ABSTRACT Purpose: This study aimed to analyze the clinical patterns and etiology of uveitis in Isfahan, Iran. Methods: In this descriptive research, the records of 2016 patients with uveitis referred to a tertiary eye care centers were examined. Age, sex, clinical and anatomical features, and etiology of disease were recorded and analyzed. Results: The mean age of onset of uveitis was 33.76 years and the women/men ratio was 1.2/1.0. Anterior uveitis was the most common (42.9%) type followed by posterior (21.4%), intermediate (19.3%), and pan uveitis (16.31%). Noninfectious causes had more roles (76.5%) in the etiology of uveitis. A total of 43.9% of the patients had unknown etiology (idiopathic). The most common known etiologies were toxoplasmosis, Behc¸et disease and Fuchs heterochromic iridiocyclitis (FHI), respectively. In 15.6%, there was an underlying systemic disease. Conclusion: There were some differences in the clinical and etiologic pattern of uveitis in Isfahan. Environmental, genetic, and geographical factors may contribute to this difference. Keywords: Causes, clinical pattern, epidemiology, Isfahan, Iran, uveitis
the disease has been changing.2 For indicating uveitis clinical pattern in Isfahan, Iran, this retrospective study was conducted to assess the changes during 13 years; the results were compared with those of different models from other countries.
Uveitis is among the most important diseases in ophthalmology; 10–15% of cases of legal blindness in developed countries are due to uveitis.1 Most of the cases are in the active ages of life (20–60 years) and major complications, such as cataracts, glaucoma, iris adhesion, and cystoid macular edema, are common among them. So, early detection and timely treatment are of great importance.2 Epidemiological studies indicate the importance and extent of the disease in different societies.3 In the year 2000 in Iran, an epidemiologic study of uveitis was conducted in the center of Labbafinejad in Tehran.4 The first report of uveitis was published in 2004 in Isfahan.5 Over the years, the epidemiology of
METHODS AND MATERIALS In this retrospective descriptive study, all the records of the patients referred to uvea clinics in Isfahan Feiz Eye Hospital since the founding of inflammatory eye disease clinics (in 1999) until 2012 were surveyed. During this period, approximately 2016 patients were
Received 9 February 2014; revised 26 February 2014; accepted 5 March 2014; published online 14 April 2014 Correspondence: Zahra Mohammadi, MD, Isfahan Eye Research Center, Feiz Eye Hospital, Isfahan University of Medical Sciences, Isfahan, Iran. E-mail: [email protected]
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Uveitis in an Iranian Tertiary Eye Center referred to the clinic and retina and vitreous subspecialists examined all of them. Information about age, gender, clinical and anatomic features, and etiology (co-morbidities) were recorded in patient files. The study was performed in compliance with Helsinki declaration after approval by the institutional review board of Feiz Hospital. Anatomic diagnosis of the disease was made according to the SUN Working Group Anatomical Classification of Uveitis, and in four groups—anterior, posterior, intermediate, and pan uveitis.6 To detect a patient’s underlying disease, depending on the case, required tests were performed, such as complete blood count (CBC), erythrocyte sedimentation rate (ESR), urinalysis, chest x-ray (CXR), and purified protein derivative (PPD) skin test. Further tests were performed according to need, including human leukocyte antigen (HLA) typing, assessment of angiotensin-converting enzyme (ACE), antinuclear antibody (ANA), and anti-neutrophil cytoplasmic antibody (ANCA) levels, VDRL (Venereal Disease Research Laboratory test), PCR (polymerase chain reaction), sputum culture and direct sputum smear, sacroiliac and sinus radiographs, high-resolution CT chest, and cutaneous and mucosal biopsies. If necessary, the advice of other specialists, particularly in rheumatology and infectious diseases, was used to confirm systemic disease. Diagnosis of uveitis and its relationship with systemic disease as a definitive diagnosis was made. The term ‘‘unknown’’ was applied to cases in which specific eye cause or an underlying systemic disease was not found. The researcher carried out the final patient follow-up and diagnosis.
RESULTS During the study period, 2016 patients were studied, of which 915 (45.4%) were men and 1101 (54.6%) were women. The mean age was 33.76 ± 10.56 years, and the youngest and the oldest patients were 2.5 and 98 years old, respectively. The age distribution of the patients
279
showed that the most common age for uveitis was the fourth decade of life, approximately 28.4% of the population. Based on the anatomic segmentation, anterior uveitis, with prevalence of 43%, was the most common type, followed by posterior uveitis with 21.4%, intermediate uveitis with 19.3%, and finally panuveitis with 16.31%. Results based on time course, type of inflammation, infectious or noninfectious, and ocular involvement according to uveitis type are shown in Table 1. As can be seen, the disease has an acute process in most cases (42.9%). So, overall, 23% of the patients had acute anterior uveitis and 18.5% were suffering from acute posterior uveitis. Note that in intermediate (90.7%) and posterior uveitis (90.03%), most of the cases were in chronic condition (Table 2). According to the type of granulomatosis, uveitis was nongranulomatous in 91.3% of the cases and granulomatous in 8.7% of the cases. This ratio was almost identical in all types of uveitis. In terms of etiology, the cause responsible for the disease was infection in 23.5% of the cases and noninfectious in 76.5% of them. In posterior uveitis, in 88.6% of cases the etiology was infection, while in other types of anatomical uveitis, the infectious causes accounted for a smaller percentage. In 61.1% of the cases, uveitis was unilateral and the direction of the involvement in the eyes was almost equal in both eyes. In anterior and posterior uveitis the disease was mostly unilateral. Nevertheless, in intermediate uveitis (76.1%) and panuveitis (74.3%) the disease was mostly bilateral. From 2016 studied patients, 1131 (56.1%) were allocated to a cause (the most likely diagnosis was considered as the diagnosis). The underlying cause of uveitis in 883 patients (43.79%) was unknown. The most common known cause was toxoplasmosis in 391 patients (19.39%), followed by Fuchs heterochromic iridocyclitis (FHI) disease in 14.13%, and Behc¸et disease in 10.50% of the patients. Most of the FHI cases were in the third and fourth decade of their lives (64.3%), and it was 1.13 times more prevalent in women than in men.
TABLE 1. Frequency distribution of patients with uveitis based on disease characteristics according to the type of uveitis. Characteristics Acute Chronic Recurrent Granulomatous Nongranulomatous Infectious Noninfectious Monocular Binocular Total
Anterior uveitis n (%) 467 340 59 78 788 81 784 686 179 865
(23.16) (16.8) (2.9) (3.8) (39.13) (4.1) (38.8) (34.02) (8.9) (42.9)
Posterior uveitis n (%) 377 (18.7) 27(1.4) 27 (1.4) 41 (2.03) 391 (19. 4) 382 (19) 50 (2.4) 369 (18.25) 63 (3) 432 (21.42)
Percentages are related to all patients that participated in the research. Copyright ! 2015 Taylor & Francis Group, LLC
Intermediate uveitis n (%) 34 354 2 22 368 2 388 92 298 390
(1.6) (17.6) (0.05) (1.14) (18.15) (0.09) (19.24) (4.6) (14.7) (19.3)
Panuveitis n (%) 44 281 4 35 294 9 320 85 244 329
(2.18) (13.93) (0.1) (1.68) (14.58) (0.4) (15.9) (4.2) (12.1) (16.3)
Total n (%) 922 (45.55) 1002 (49.6) 92 (4.5) 176 (8.7) 1840 (91.2) 474 (23.5) 1542 (76.5) 1232 (61.1) 784 (38.9) 2016
280 F. Kianersi et al. TABLE 2. Frequency distribution of patients with uveitis based on disease characteristics according to the type of uveitis (based on the number of individuals related to anatomical classification). Characteristics Acute Chronic Recurrent Granulomatous Nongranulomatous Infectious Noninfectious Monocular Binocular
Anterior uveitis %
Posterior uveitis %
Intermediate uveitism %
Pan uveitis %
8.8 90.7 0.5 5.6 94.4 0.5 99.5 23.6 76.4
87.26 6.25 6.25 9.4 90.5 88.4 11.57 85.4 14.5
54 39.3 6.8 9.1 90.9 9.36 90.6 79.3 20.6
13.37 85.4 1.2 10.6 89.3 2.7 97.26 25.8 74.2
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TABLE 3. Patient distribution according to systemic disease based on gender differentiation. Women Men (n) (n) Total
Systemic disease Behc¸et disease Juvenile rheumatoid arthritis Psoriasis Rheumatoid arthritis Lupus Wegener granulomatosis Ulcerative colitis HLA-B27 (human leukocyte antigen B27)-associated uveitis Tuberculosis Brucellosis Sarcoidosis Vogt-Koyanagi-Harada (VKH) Multiple sclerosis (MS) Lymphoma Total
Total (of 2016 patients) n (%) 922 1002 92 176 1840 474 1542 1232 784
(45.55) (49.6) (4.5) (8.7) (91.2) (23.5) (76.5) (61.1) (38.9)
TABLE 4. Frequency distribution of anterior uveitis according to the etiology. n
%
437 285 66 8 11 11 6 23 2 5 4 4 3 865
50.5 32.8 7.6 1.01 1.3 1.3 0.22 2.6 0.2 0.6 0.5 0.5 0.3 100
Etiology %
101 10 2 6 1 0 1 6
111 8 2 6 3 1 3 4
212 18 4 12 4 1 4 10
10.51 0.90 0.19 0.56 0.19 0.04 0.19 0.496
3 1 8 10 10 0 159
1 0 3 4 6 2 154
4 1 11 14 16 2 313
0.19 0.04 0.54 0.694 0.80 0.1 15.52
Eye inflammation in 315 patients (15.52%) was observed in association with a systemic disease. Table 3 shows the frequency distribution and percentage of systemic diseases with uveitis, mean age, and gender distribution. Tables 4–7 identify the distribution of uveitis disease causes according to the anatomic classification.
DISCUSSION In the present study, the mean age of people with uveitis was 33.76 ± 10.56 years with a range of 2.5–98 years. In some other studies conducted in different parts of the world, the mean age was about 35 years.4,7–10 In our study, the maximum incidence of the disease was in the third and fourth decades of life. The ratio of women to men was 1.2/1 in the present study, which is different from that of a study in Turkey (1/1.04)10 and a study in Saudi Arabia (0.6/1),7 while the results of Eastern Europe were similar to those of the present study (1.14/1).11
Idiopathic Fuchs heterochromic iridocyclitis (FHI) Herpes simplex Ankylosing spondylitis Juvenile rheumatoid arthritis Adenovirus Rheumatoid arthritis Behc¸et disease Scleritis Varicella zoster virus (VZV) Trauma Lupus Ulcerative colitis Total
TABLE 5. Frequency distribution of intermediate uveitis according to etiology. Etiology Idiopathic Tuberculosis Multiple sclerosis Sarcoidosis Behc¸et disease Rheumatoid arthritis Retinitis pigmentosa Juvenile rheumatoid arthritis (JRA) Retinal detachment (RD) Foreign body in the eye Psoriasis Total
n
%
319 2 16 4 24 5 8 5 3 2 2 390
81.58 0.5 4.1 1.00 6.1 1.20 2.04 1.20 0.76 0.5 0.5 100
Chronic uveitis (49.6%), nongranulomatous uveitis (91.2%), and noninfectious uveitis (76.5%) were the most common types of uveitis in our study. In a study by Soheilian et al. in Tehran, Iran, chronic uveitis (62.1%), noninfectious uveitis (83.5%), and nongranulomatous uveitis (85.5%) were the most common types of uveitis.4 Rudriguez et al. in America also showed that chronic uveitis (53.8%), noninfectious Ocular Immunology & Inflammation
Uveitis in an Iranian Tertiary Eye Center uveitis (77.7%), and nongranulomatous uveitis (83.1%) were the most common types.9 The distribution of different forms of uveitis in the present study were very similar to the past studies conducted in different places.12 In terms of location, anterior uveitis was the most common type (42.9%) in the present study followed by posterior uveitis (21.42%), intermediate uveitis (19.3%), and panuveitis (16.31%). However, these figures were different from the figures obtained in Soheilian et al.4 study in TABLE 6. Frequency distribution of posterior uveitis according to etiology. n
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Etiology
%
Idiopathic 20 4.7 Toxoplasmosis 391 90.7 Behc¸et disease 6 1.4 Harada 4 0.9 Birdshot 2 0.5 Toxocara 1 0.2 Rheumatoid arthritis 1 0.2 Ulcerative colitis 1 0.2 Human immunodeficiency virus (HIV) 1 0.2 Cytomegalovirous (CMV) 4 0.5 MEWDS (multiple evanescent white dot syndrome) 1 0.2 Total 432 100
TABLE 7. Frequency distribution of pan uveitis according to etiology. Etiology Idiopathic Behc¸et disease Vogkt-Koyanagi-Harada (VKH) Birdshot Juvenile rheumatoid arthritis Retinal detachment (RD) Trauma Eales disease Sympathetic ophthalmia Acute retina necrosis (ARN) Endophthalmitis Ankylosing spondylitis Sarcoidosis Rheumatoid arthritis Tuberculosis Psoriasis Brucellosis Lymphoma Wegener’s granulomatosis Total
n
%
106 159 9 2 2 5 2 5 7 8 5 2 8 1 2 2 1 2 1 329
32 48 2.7 0.3 1.2 1.5 0.3 1.5 1.8 2.4 0.3 0.6 2.4 0.3 0.6 0.6 0.3 0.6 0.3 100
281
Tehran. This difference was probably due to the difference in climate and race of Iranian people (Table 8). In terms of time segmentation, the most common type was chronic uveitis (49.6%), which was quite similar to Soheilian et al.4 study in Tehran. This similarity might be due to conducting the study in referral centers, as other ophthalmologists treated most of the acute and anterior uveitis and did not refer them. On the other hand, recurrent uveitis in the present study had a prevalence of 4.5% among all the patients. In anterior uveitis, 6.81% of the cases became recurrent. In the Soheilian et al. study, 16.7% of patients were suffering from recurrent anterior uveitis.4 Noninfectious cause was the most common etiology of uveitis in the present study, which was the same as other studies as well.4,7,8 In posterior uveitis most infectious cases (88.57%) were seen, while in other anatomic types, infectious cause was the lesser reason for uveitis. In 43.89% of the cases, the cause of uveitis was unknown (idiopathic), while in the Michclokis et al. study16 27.6% and in the Sengun et al. study14 28.3% of the cases were unknown. The most common cause of uveitis in the present study was toxoplasmosis, with a prevalence of 19.4% (391 patients). In other studies, toxoplasmosis in the etiology of uveitis had 0.5–17.4% of prevelance.4,5,7,12 Prevalence of toxoplasmosis in the present study was slightly higher than in other studies. In other research in the present center, prevalence of ocular toxoplasmosis was 19.3% among 1000 patients.17 The reason for this is the abundance of contamination of the Toxoplasma parasite in Isfahan. In this study, the most common noninfectious cause of uveitis was Behc¸et disease (approximately 10.5%). This amount is more than the amount in the Islam and Tabbara research (6.5%)7 in Saudi Arabia but lower than that of the Kazokoglu et al. study (32.1%) in Turkey.10 Perhaps, the reason is due to the prevalence of the disease in Turkey, while the obtained prevalence is almost the same as that of the Soheilian et al. study in Tehran (8.6%).4 Different reports have shown the share of etiology in this disease to be 2.5–26%.8,12 Diagnosed systemic disease as a cause of the uveitis had a share of 15.62% of the patients in this study. In our study JRA (juvenile rheumatoid arteritis) had prevalence about 0.4% and HLA-B27 (human leukocyte antigen B27)-associated uveitis had 0/94%,
TABLE 8. The distribution of different forms of uveitis in different research studies. Types of uveitis Anterior Posterior Intermediate Pan uveitis
Guex 1999, Sengun 2005, Merecanti 2001, Present Soheilian 2001, Paivonsalo 1994, Wakabayashi 2003, Finland (%)8 Japan (%)12 Sweden, (%)13 Turkey (%)14 Italy (%)15 research (%) Tehran (%)4 42.9 21.4 19.3 16.31
38.4 18.6 17.6 25.4
Copyright ! 2015 Taylor & Francis Group, LLC
92.2 5.7 1.3 0.8
29.6 31.2 6.9 30.7
47 21 12 20
43.6 26.6 9 20.6
58.1 36.1 2.9 12.98
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282 F. Kianersi et al. while in other parts of world these entities were more prevalent.9,15 Uveitis with unknown etiology (pars planitis) was the most common cause of intermediate uveitis (82.2%), which is similar to other studies.4 Other common causes of intermediate uveitis in this study were Behc¸et disease with 6.2% prevalence and multiple sclerosis (MS) with a prevalence of 4.12%. From 4 patients studied with tuberculosis (TB), 2 had severe vitritis with mild signs of inflammation in the anterior chamber and the retina was not affected, so they were considered as having intermediate uveitis, but the other two had panuveitis. TB treatment was performed on 4 cases; with the recovery of systemic symptoms, visual symptoms were also improved and there was no recurrence during the study. In our study, the most common cause for panuveitis was Behc¸et disease (48.03%), followed by unknown reason (32.02%). In the Soheilian et al. study, Behc¸et disease was also the most important cause for panuveitis (47%).4 The higher prevalence of this disease in Isfahan might be due to more referring of the patients with Behc¸et disease to the uvea clinic. Vogt-Koyanagi-Harada (VKH) disease, with a prevalence of 3.02%, was the third most common cause of panuveitis. In many studies, such as Das et al. in India, this disease is reported as the most common cause of panuveitis.18 In this study, 20 cases were reported with masquerade syndrome and 8 of them were diagnosed with retinal detachment (RD). Five were referred with diagnosis of panuveitis; among them, 2 patients had Coats disease and 3 others were suffering from rhegmatogenous retinal detachment. Two patients had intraocular foreign bodies and were diagnosed with intermediate uveitis, and the others were suffering from retinitis pigmentosa (RP) and lymphoma. There was also a child with brucellosis in this study, who was referred to the clinic due to panuveitis. He was treated with topical and systemic corticosteroids and the treatment for brucellosis. Any recurrence was not observed during the study.
CONCLUSION The epidemiology of uveitis in this study has some differences from other studies. The prevalence of Fuchs disease, Behc¸et disease, and toxoplasmosis was different and greater in the present study and their association with HLA-B27-associated uveitis and juvenile rheumatoid arthritis was less.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
REFERENCES 1. Cunningham E, Crawford B. Uveal tract and sclera. In: Vaughan D, Asbury T, eds. Riordan-Eva General Ophthalmology, 17th ed. San Francisco: Appleton & Lange; 1999:142–158. 2. Rao N, Cousios S, Froster D, Opromcol M. Clinical approach to uveitis. In: American Academy of Ophthalmology. Basic and Clinical Science Course, Section 9: Intraocular Inflammation and Uveitis. San Francisco: American Academy of Ophthalmology; 2010-2011:100–146. 3. Smith RL, Baarsma GS. Epidemiology of uveitis. Curr Opin Ophthalmol. 1995;6:57–61. 4. Soheilian M, Heidari K, Yazdani S, et al. Patterns of uveitis in a tertiary eye care center in Iran. Ocul Immunol Inflamm. 2004;12:297–310. 5. Kianersi F. Clinical patterns of uveitis in an Iranian tertiary eye care center. [In Farsi] Bina Ophthalmol. 2005;10:147–145. 6. Jabs DA, Nussenblatt RB, Rosenbaum JT. the Standardization of Uveitis Nomenclature (SUN) Working Group. Standardization of uveitis nomenclature for reporting clinical data: results of the First International Workshop. Am J Ophthalmol. 2005;140:509–516. 7. Islam SM, Tabbara KF. Causes of uveitis at the eye center in Saudi Arabia: a retrospective review. Ophthalm Epidmiol. 2002;9:239–249. 8. Paivonsalo-Hietanen T, Vaahtoranta-Lehtonen H, Tuominen J, et al. Uveitis survey at the University Eye Clinic in Turku. Ophtalmol (Copenh). 1994;72:505–512. 9. Rudriguez A, Claonge M, Pedroza-Seres M, et al. Referral patterns of uveitis in a tertiary eye care center. Arch Ophthalmol. 1996;114:593–599. 10. Kazokoglu H, Onal S. Tugal-Tutkun I, et al. Demographic and clinical features of uveitis in tertiary centers in Turkey. Apaydin Ophthalm Epidemiol. 2008;15:285–293. 11. Biziorek B, Mackiewicz J, Zago´rski Z, et al. Etiology of uveitis in rural and urban areas of mid-eastern Poland. Ann Agric Environ Med. 2001;8:241–243. 12. Wakabayash TI, Morimura Y, Miyamoto Y, et al. Changing patterns of intraocular inflanmatory disease in Japan. Ocul Immunol Inflamm. 2003;11:277–286. 13. Guex-Crosie Y. Epidemiology of uveitis. Rav Practicien. 1999;49:1989–1995. 14. Sengun A, Karadag R, Karakurt A. Cause of uveitis in a referral hospital in Ankara, Turkey. Ocul Immunol Inflamm. 2005;1:45–50. 15. Mercanti A, Parolini B, Benoro A, et al. Epidemiology of endogenous uveitis in north-eastern Italy: analysis of 655 new cases. Acta Ophthalmol Scand. 2001;19:64–68. 16. Michclokis ME, Chrysomalakou M, Karavella P, et al. Clinical patterns of uveitis in a Greek tertiary eye care center. Greek Ann Ophthalmol. 1998;l:43–55. 17. Kianersi F, Naderi Beni A, Naderi Beni Z. Clinical manifestation and prognosis of active ocular toxoplasmosis in Iran. Int Ophthalmol. 2012;32:539–545. 18. Das D, Biswas J, Ganesh SK. Pattern of uveitis in a referral uveitis clinic in India. Indian J Ophthalmol. 1995;43:117–121.
Ocular Immunology & Inflammation
ISSN: 0927-3948 (Print) 1744-5078 (Online) Journal homepage: http://www.tandfonline.com/loi/ioii20
Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center Farzan Kianersi MD, Zahra Mohammadi MD, Heshmatollah Ghanbari MD, Seyed Mohammad Ghoreyshi MD, Hadi Karimzadeh MD & Masoud Soheilian MD To cite this article: Farzan Kianersi MD, Zahra Mohammadi MD, Heshmatollah Ghanbari MD, Seyed Mohammad Ghoreyshi MD, Hadi Karimzadeh MD & Masoud Soheilian MD (2015) Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center, Ocular Immunology and Inflammation, 23:4, 278-282, DOI: 10.3109/09273948.2014.902474 To link to this article: http://dx.doi.org/10.3109/09273948.2014.902474
Published online: 16 Apr 2014.
Submit your article to this journal
Article views: 56
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ioii20 Download by: [University of Michigan]
Date: 21 September 2015, At: 23:38
Ocular Immunology & Inflammation, 2015; 23(4): 278–282 Copyright ! Taylor & Francis Group, LLC ISSN: 0927-3948 print / 1744-5078 online DOI: 10.3109/09273948.2014.902474
ORIGINAL ARTICLE
Clinical Patterns of Uveitis in an Iranian Tertiary Eye-care Center Farzan Kianersi, MD1, Zahra Mohammadi, MD2, Heshmatollah Ghanbari, Seyed Mohammad Ghoreyshi, MD1,3, Hadi Karimzadeh, MD3, and Masoud Soheilian, MD4
MD
1
,
Downloaded by [University of Michigan] at 23:38 21 September 2015
1
Department of Ophthalmology, School of Medicine, Isfahan University of Medical Science, Isfahan, Iran, 2 Isfahan Eye Research Center, Feiz Eye Hospital, Isfahan University of Medical Sciences, Isfahan, Iran, 3 Department of Rheumatology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran, and 4Department of Ophthalmology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
ABSTRACT Purpose: This study aimed to analyze the clinical patterns and etiology of uveitis in Isfahan, Iran. Methods: In this descriptive research, the records of 2016 patients with uveitis referred to a tertiary eye care centers were examined. Age, sex, clinical and anatomical features, and etiology of disease were recorded and analyzed. Results: The mean age of onset of uveitis was 33.76 years and the women/men ratio was 1.2/1.0. Anterior uveitis was the most common (42.9%) type followed by posterior (21.4%), intermediate (19.3%), and pan uveitis (16.31%). Noninfectious causes had more roles (76.5%) in the etiology of uveitis. A total of 43.9% of the patients had unknown etiology (idiopathic). The most common known etiologies were toxoplasmosis, Behc¸et disease and Fuchs heterochromic iridiocyclitis (FHI), respectively. In 15.6%, there was an underlying systemic disease. Conclusion: There were some differences in the clinical and etiologic pattern of uveitis in Isfahan. Environmental, genetic, and geographical factors may contribute to this difference. Keywords: Causes, clinical pattern, epidemiology, Isfahan, Iran, uveitis
the disease has been changing.2 For indicating uveitis clinical pattern in Isfahan, Iran, this retrospective study was conducted to assess the changes during 13 years; the results were compared with those of different models from other countries.
Uveitis is among the most important diseases in ophthalmology; 10–15% of cases of legal blindness in developed countries are due to uveitis.1 Most of the cases are in the active ages of life (20–60 years) and major complications, such as cataracts, glaucoma, iris adhesion, and cystoid macular edema, are common among them. So, early detection and timely treatment are of great importance.2 Epidemiological studies indicate the importance and extent of the disease in different societies.3 In the year 2000 in Iran, an epidemiologic study of uveitis was conducted in the center of Labbafinejad in Tehran.4 The first report of uveitis was published in 2004 in Isfahan.5 Over the years, the epidemiology of
METHODS AND MATERIALS In this retrospective descriptive study, all the records of the patients referred to uvea clinics in Isfahan Feiz Eye Hospital since the founding of inflammatory eye disease clinics (in 1999) until 2012 were surveyed. During this period, approximately 2016 patients were
Received 9 February 2014; revised 26 February 2014; accepted 5 March 2014; published online 14 April 2014 Correspondence: Zahra Mohammadi, MD, Isfahan Eye Research Center, Feiz Eye Hospital, Isfahan University of Medical Sciences, Isfahan, Iran. E-mail: [email protected]
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Uveitis in an Iranian Tertiary Eye Center referred to the clinic and retina and vitreous subspecialists examined all of them. Information about age, gender, clinical and anatomic features, and etiology (co-morbidities) were recorded in patient files. The study was performed in compliance with Helsinki declaration after approval by the institutional review board of Feiz Hospital. Anatomic diagnosis of the disease was made according to the SUN Working Group Anatomical Classification of Uveitis, and in four groups—anterior, posterior, intermediate, and pan uveitis.6 To detect a patient’s underlying disease, depending on the case, required tests were performed, such as complete blood count (CBC), erythrocyte sedimentation rate (ESR), urinalysis, chest x-ray (CXR), and purified protein derivative (PPD) skin test. Further tests were performed according to need, including human leukocyte antigen (HLA) typing, assessment of angiotensin-converting enzyme (ACE), antinuclear antibody (ANA), and anti-neutrophil cytoplasmic antibody (ANCA) levels, VDRL (Venereal Disease Research Laboratory test), PCR (polymerase chain reaction), sputum culture and direct sputum smear, sacroiliac and sinus radiographs, high-resolution CT chest, and cutaneous and mucosal biopsies. If necessary, the advice of other specialists, particularly in rheumatology and infectious diseases, was used to confirm systemic disease. Diagnosis of uveitis and its relationship with systemic disease as a definitive diagnosis was made. The term ‘‘unknown’’ was applied to cases in which specific eye cause or an underlying systemic disease was not found. The researcher carried out the final patient follow-up and diagnosis.
RESULTS During the study period, 2016 patients were studied, of which 915 (45.4%) were men and 1101 (54.6%) were women. The mean age was 33.76 ± 10.56 years, and the youngest and the oldest patients were 2.5 and 98 years old, respectively. The age distribution of the patients
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showed that the most common age for uveitis was the fourth decade of life, approximately 28.4% of the population. Based on the anatomic segmentation, anterior uveitis, with prevalence of 43%, was the most common type, followed by posterior uveitis with 21.4%, intermediate uveitis with 19.3%, and finally panuveitis with 16.31%. Results based on time course, type of inflammation, infectious or noninfectious, and ocular involvement according to uveitis type are shown in Table 1. As can be seen, the disease has an acute process in most cases (42.9%). So, overall, 23% of the patients had acute anterior uveitis and 18.5% were suffering from acute posterior uveitis. Note that in intermediate (90.7%) and posterior uveitis (90.03%), most of the cases were in chronic condition (Table 2). According to the type of granulomatosis, uveitis was nongranulomatous in 91.3% of the cases and granulomatous in 8.7% of the cases. This ratio was almost identical in all types of uveitis. In terms of etiology, the cause responsible for the disease was infection in 23.5% of the cases and noninfectious in 76.5% of them. In posterior uveitis, in 88.6% of cases the etiology was infection, while in other types of anatomical uveitis, the infectious causes accounted for a smaller percentage. In 61.1% of the cases, uveitis was unilateral and the direction of the involvement in the eyes was almost equal in both eyes. In anterior and posterior uveitis the disease was mostly unilateral. Nevertheless, in intermediate uveitis (76.1%) and panuveitis (74.3%) the disease was mostly bilateral. From 2016 studied patients, 1131 (56.1%) were allocated to a cause (the most likely diagnosis was considered as the diagnosis). The underlying cause of uveitis in 883 patients (43.79%) was unknown. The most common known cause was toxoplasmosis in 391 patients (19.39%), followed by Fuchs heterochromic iridocyclitis (FHI) disease in 14.13%, and Behc¸et disease in 10.50% of the patients. Most of the FHI cases were in the third and fourth decade of their lives (64.3%), and it was 1.13 times more prevalent in women than in men.
TABLE 1. Frequency distribution of patients with uveitis based on disease characteristics according to the type of uveitis. Characteristics Acute Chronic Recurrent Granulomatous Nongranulomatous Infectious Noninfectious Monocular Binocular Total
Anterior uveitis n (%) 467 340 59 78 788 81 784 686 179 865
(23.16) (16.8) (2.9) (3.8) (39.13) (4.1) (38.8) (34.02) (8.9) (42.9)
Posterior uveitis n (%) 377 (18.7) 27(1.4) 27 (1.4) 41 (2.03) 391 (19. 4) 382 (19) 50 (2.4) 369 (18.25) 63 (3) 432 (21.42)
Percentages are related to all patients that participated in the research. Copyright ! 2015 Taylor & Francis Group, LLC
Intermediate uveitis n (%) 34 354 2 22 368 2 388 92 298 390
(1.6) (17.6) (0.05) (1.14) (18.15) (0.09) (19.24) (4.6) (14.7) (19.3)
Panuveitis n (%) 44 281 4 35 294 9 320 85 244 329
(2.18) (13.93) (0.1) (1.68) (14.58) (0.4) (15.9) (4.2) (12.1) (16.3)
Total n (%) 922 (45.55) 1002 (49.6) 92 (4.5) 176 (8.7) 1840 (91.2) 474 (23.5) 1542 (76.5) 1232 (61.1) 784 (38.9) 2016
280 F. Kianersi et al. TABLE 2. Frequency distribution of patients with uveitis based on disease characteristics according to the type of uveitis (based on the number of individuals related to anatomical classification). Characteristics Acute Chronic Recurrent Granulomatous Nongranulomatous Infectious Noninfectious Monocular Binocular
Anterior uveitis %
Posterior uveitis %
Intermediate uveitism %
Pan uveitis %
8.8 90.7 0.5 5.6 94.4 0.5 99.5 23.6 76.4
87.26 6.25 6.25 9.4 90.5 88.4 11.57 85.4 14.5
54 39.3 6.8 9.1 90.9 9.36 90.6 79.3 20.6
13.37 85.4 1.2 10.6 89.3 2.7 97.26 25.8 74.2
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TABLE 3. Patient distribution according to systemic disease based on gender differentiation. Women Men (n) (n) Total
Systemic disease Behc¸et disease Juvenile rheumatoid arthritis Psoriasis Rheumatoid arthritis Lupus Wegener granulomatosis Ulcerative colitis HLA-B27 (human leukocyte antigen B27)-associated uveitis Tuberculosis Brucellosis Sarcoidosis Vogt-Koyanagi-Harada (VKH) Multiple sclerosis (MS) Lymphoma Total
Total (of 2016 patients) n (%) 922 1002 92 176 1840 474 1542 1232 784
(45.55) (49.6) (4.5) (8.7) (91.2) (23.5) (76.5) (61.1) (38.9)
TABLE 4. Frequency distribution of anterior uveitis according to the etiology. n
%
437 285 66 8 11 11 6 23 2 5 4 4 3 865
50.5 32.8 7.6 1.01 1.3 1.3 0.22 2.6 0.2 0.6 0.5 0.5 0.3 100
Etiology %
101 10 2 6 1 0 1 6
111 8 2 6 3 1 3 4
212 18 4 12 4 1 4 10
10.51 0.90 0.19 0.56 0.19 0.04 0.19 0.496
3 1 8 10 10 0 159
1 0 3 4 6 2 154
4 1 11 14 16 2 313
0.19 0.04 0.54 0.694 0.80 0.1 15.52
Eye inflammation in 315 patients (15.52%) was observed in association with a systemic disease. Table 3 shows the frequency distribution and percentage of systemic diseases with uveitis, mean age, and gender distribution. Tables 4–7 identify the distribution of uveitis disease causes according to the anatomic classification.
DISCUSSION In the present study, the mean age of people with uveitis was 33.76 ± 10.56 years with a range of 2.5–98 years. In some other studies conducted in different parts of the world, the mean age was about 35 years.4,7–10 In our study, the maximum incidence of the disease was in the third and fourth decades of life. The ratio of women to men was 1.2/1 in the present study, which is different from that of a study in Turkey (1/1.04)10 and a study in Saudi Arabia (0.6/1),7 while the results of Eastern Europe were similar to those of the present study (1.14/1).11
Idiopathic Fuchs heterochromic iridocyclitis (FHI) Herpes simplex Ankylosing spondylitis Juvenile rheumatoid arthritis Adenovirus Rheumatoid arthritis Behc¸et disease Scleritis Varicella zoster virus (VZV) Trauma Lupus Ulcerative colitis Total
TABLE 5. Frequency distribution of intermediate uveitis according to etiology. Etiology Idiopathic Tuberculosis Multiple sclerosis Sarcoidosis Behc¸et disease Rheumatoid arthritis Retinitis pigmentosa Juvenile rheumatoid arthritis (JRA) Retinal detachment (RD) Foreign body in the eye Psoriasis Total
n
%
319 2 16 4 24 5 8 5 3 2 2 390
81.58 0.5 4.1 1.00 6.1 1.20 2.04 1.20 0.76 0.5 0.5 100
Chronic uveitis (49.6%), nongranulomatous uveitis (91.2%), and noninfectious uveitis (76.5%) were the most common types of uveitis in our study. In a study by Soheilian et al. in Tehran, Iran, chronic uveitis (62.1%), noninfectious uveitis (83.5%), and nongranulomatous uveitis (85.5%) were the most common types of uveitis.4 Rudriguez et al. in America also showed that chronic uveitis (53.8%), noninfectious Ocular Immunology & Inflammation
Uveitis in an Iranian Tertiary Eye Center uveitis (77.7%), and nongranulomatous uveitis (83.1%) were the most common types.9 The distribution of different forms of uveitis in the present study were very similar to the past studies conducted in different places.12 In terms of location, anterior uveitis was the most common type (42.9%) in the present study followed by posterior uveitis (21.42%), intermediate uveitis (19.3%), and panuveitis (16.31%). However, these figures were different from the figures obtained in Soheilian et al.4 study in TABLE 6. Frequency distribution of posterior uveitis according to etiology. n
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Etiology
%
Idiopathic 20 4.7 Toxoplasmosis 391 90.7 Behc¸et disease 6 1.4 Harada 4 0.9 Birdshot 2 0.5 Toxocara 1 0.2 Rheumatoid arthritis 1 0.2 Ulcerative colitis 1 0.2 Human immunodeficiency virus (HIV) 1 0.2 Cytomegalovirous (CMV) 4 0.5 MEWDS (multiple evanescent white dot syndrome) 1 0.2 Total 432 100
TABLE 7. Frequency distribution of pan uveitis according to etiology. Etiology Idiopathic Behc¸et disease Vogkt-Koyanagi-Harada (VKH) Birdshot Juvenile rheumatoid arthritis Retinal detachment (RD) Trauma Eales disease Sympathetic ophthalmia Acute retina necrosis (ARN) Endophthalmitis Ankylosing spondylitis Sarcoidosis Rheumatoid arthritis Tuberculosis Psoriasis Brucellosis Lymphoma Wegener’s granulomatosis Total
n
%
106 159 9 2 2 5 2 5 7 8 5 2 8 1 2 2 1 2 1 329
32 48 2.7 0.3 1.2 1.5 0.3 1.5 1.8 2.4 0.3 0.6 2.4 0.3 0.6 0.6 0.3 0.6 0.3 100
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Tehran. This difference was probably due to the difference in climate and race of Iranian people (Table 8). In terms of time segmentation, the most common type was chronic uveitis (49.6%), which was quite similar to Soheilian et al.4 study in Tehran. This similarity might be due to conducting the study in referral centers, as other ophthalmologists treated most of the acute and anterior uveitis and did not refer them. On the other hand, recurrent uveitis in the present study had a prevalence of 4.5% among all the patients. In anterior uveitis, 6.81% of the cases became recurrent. In the Soheilian et al. study, 16.7% of patients were suffering from recurrent anterior uveitis.4 Noninfectious cause was the most common etiology of uveitis in the present study, which was the same as other studies as well.4,7,8 In posterior uveitis most infectious cases (88.57%) were seen, while in other anatomic types, infectious cause was the lesser reason for uveitis. In 43.89% of the cases, the cause of uveitis was unknown (idiopathic), while in the Michclokis et al. study16 27.6% and in the Sengun et al. study14 28.3% of the cases were unknown. The most common cause of uveitis in the present study was toxoplasmosis, with a prevalence of 19.4% (391 patients). In other studies, toxoplasmosis in the etiology of uveitis had 0.5–17.4% of prevelance.4,5,7,12 Prevalence of toxoplasmosis in the present study was slightly higher than in other studies. In other research in the present center, prevalence of ocular toxoplasmosis was 19.3% among 1000 patients.17 The reason for this is the abundance of contamination of the Toxoplasma parasite in Isfahan. In this study, the most common noninfectious cause of uveitis was Behc¸et disease (approximately 10.5%). This amount is more than the amount in the Islam and Tabbara research (6.5%)7 in Saudi Arabia but lower than that of the Kazokoglu et al. study (32.1%) in Turkey.10 Perhaps, the reason is due to the prevalence of the disease in Turkey, while the obtained prevalence is almost the same as that of the Soheilian et al. study in Tehran (8.6%).4 Different reports have shown the share of etiology in this disease to be 2.5–26%.8,12 Diagnosed systemic disease as a cause of the uveitis had a share of 15.62% of the patients in this study. In our study JRA (juvenile rheumatoid arteritis) had prevalence about 0.4% and HLA-B27 (human leukocyte antigen B27)-associated uveitis had 0/94%,
TABLE 8. The distribution of different forms of uveitis in different research studies. Types of uveitis Anterior Posterior Intermediate Pan uveitis
Guex 1999, Sengun 2005, Merecanti 2001, Present Soheilian 2001, Paivonsalo 1994, Wakabayashi 2003, Finland (%)8 Japan (%)12 Sweden, (%)13 Turkey (%)14 Italy (%)15 research (%) Tehran (%)4 42.9 21.4 19.3 16.31
38.4 18.6 17.6 25.4
Copyright ! 2015 Taylor & Francis Group, LLC
92.2 5.7 1.3 0.8
29.6 31.2 6.9 30.7
47 21 12 20
43.6 26.6 9 20.6
58.1 36.1 2.9 12.98
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282 F. Kianersi et al. while in other parts of world these entities were more prevalent.9,15 Uveitis with unknown etiology (pars planitis) was the most common cause of intermediate uveitis (82.2%), which is similar to other studies.4 Other common causes of intermediate uveitis in this study were Behc¸et disease with 6.2% prevalence and multiple sclerosis (MS) with a prevalence of 4.12%. From 4 patients studied with tuberculosis (TB), 2 had severe vitritis with mild signs of inflammation in the anterior chamber and the retina was not affected, so they were considered as having intermediate uveitis, but the other two had panuveitis. TB treatment was performed on 4 cases; with the recovery of systemic symptoms, visual symptoms were also improved and there was no recurrence during the study. In our study, the most common cause for panuveitis was Behc¸et disease (48.03%), followed by unknown reason (32.02%). In the Soheilian et al. study, Behc¸et disease was also the most important cause for panuveitis (47%).4 The higher prevalence of this disease in Isfahan might be due to more referring of the patients with Behc¸et disease to the uvea clinic. Vogt-Koyanagi-Harada (VKH) disease, with a prevalence of 3.02%, was the third most common cause of panuveitis. In many studies, such as Das et al. in India, this disease is reported as the most common cause of panuveitis.18 In this study, 20 cases were reported with masquerade syndrome and 8 of them were diagnosed with retinal detachment (RD). Five were referred with diagnosis of panuveitis; among them, 2 patients had Coats disease and 3 others were suffering from rhegmatogenous retinal detachment. Two patients had intraocular foreign bodies and were diagnosed with intermediate uveitis, and the others were suffering from retinitis pigmentosa (RP) and lymphoma. There was also a child with brucellosis in this study, who was referred to the clinic due to panuveitis. He was treated with topical and systemic corticosteroids and the treatment for brucellosis. Any recurrence was not observed during the study.
CONCLUSION The epidemiology of uveitis in this study has some differences from other studies. The prevalence of Fuchs disease, Behc¸et disease, and toxoplasmosis was different and greater in the present study and their association with HLA-B27-associated uveitis and juvenile rheumatoid arthritis was less.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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