Indian Journal of Ophthalmology

REVIEW ARTICLE
Year
: 2007  |  Volume : 55  |  Issue : 3  |  Page : 173--183

Global variation and pattern changes in epidemiology of uveitis


SR Rathinam, P Namperumalsamy 
 Aravind Eye Hospital and PG Institute of Ophthalmology, 1, Anna Nagar, Madurai - 625 020, India

Correspondence Address:
S R Rathinam
Aravind Eye Hospital and PG Institute of Ophthalmology, 1, Anna Nagar, Madurai - 625 020, Tamil Nadu
India

Abstract

Uveitis, a complex intraocular inflammatory disease results from several etiological entities. Causes of uveitis are known to vary in different populations depending upon the ecological, racial and socioeconomic variations of the population studied. Tropical countries are unique in their climate, prevailing pathogens and in the existing diseases, which further influence the epidemiological and geographical distribution of specific entities. We provide an overview of the pattern of uveitis of 15221 cases in 24 case series reported from several countries over 35 years (1972-2007) and we integrate it with our experience of an additional 8759 cases seen over six years (1996-2001) at a large community-based eye hospital. Uveitis accounted for 0.8% of our hospital-based outpatient visits. The uveitis was idiopathic in 44.6%, the most commonly identified entities in the cohort included leptospiral uveitis (9.7%), tuberculous uveitis (5.6%) and herpetic uveitis (4.9%). The most common uveitis in children below 16 years (616 patients; 7.0% of the total cohort) was pediatric parasitic anterior uveitis, (182 children, 29.5% of the pediatric cohort), whereas the most common uveitis in patients above 60 years (642 patients; 7.3% of the total cohort) was herpetic anterior uveitis, (78 patients, 12.1% of the elderly cohort). Etiologies varied with the age group of the patients. As in other tropical countries, a high prevalence of infectious uveitis was seen in this population.



How to cite this article:
Rathinam S R, Namperumalsamy P. Global variation and pattern changes in epidemiology of uveitis.Indian J Ophthalmol 2007;55:173-183


How to cite this URL:
Rathinam S R, Namperumalsamy P. Global variation and pattern changes in epidemiology of uveitis. Indian J Ophthalmol [serial online] 2007 [cited 2024 Mar 28 ];55:173-183
Available from: https://journals.lww.com/ijo/pages/default.aspx/text.asp?2007/55/3/173/31936


Full Text

Uveitis includes a large group of diverse inflammatory diseases, the frequencies of which vary considerably by geographic location around the world.[1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23] Awareness of such regional differences in the disease pattern is essential in deriving a region-specific list of differential diagnoses which in turn facilitates the final diagnosis. Factors contributing to such regional variations in the causes of uveitis are complex and incompletely understood, but include both host and environmental factors.[6],[8],[24],[25] Among the environmental factors, the most important appears to be the regional distribution of various pathogens,[24],[25],[26],[27],[28],[29] including relatively new and emerging agents. South India has a tropical climate and depends to a large extent on an agriculture-based economy. Although agricultural communities constitute a major section of the global population, accurate estimates of the causes of uveitis in such regions and populations are largely unavailable. In this paper, we present the causes and characteristics of uveitis seen over a six-year period in a large community-based eye hospital in South India and we have compared the pattern of uveitis of this population with the data from other parts of the world including the developed and developing world. [1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23]

Method of literature search

The Medline database was searched electronically using the terms uveitis, epidemiology, tropical, infectious and noninfectious uveitis. Pertinent articles from the English language literature were primarily selected. Additionally, references cited in the above articles were also gathered. Inclusion or exclusion of any article in the text was based on its relevance and usefulness.

Patients, methods and results of present study

Case records of patients examined in the uveitis clinic of a community-based eye hospital between January 1996 and December 2001, were collected for analysis. Demographic and ocular findings were recorded in a computerized database. Details on disease severity, laterality, chronicity, ocular signs and associated systemic conditions were noted. All patients had a systematic uveitis workup after a preliminary examination by a general ophthalmologist and a nonophthalmologist physician. Anatomical location of the inflammation was assigned based on the International Uveitis Study Group (IUSG) criteria.[30] The inflammation was defined as acute if symptoms were present for less than three months, chronic if symptoms were present for three months or more and recurrent if there were two or more episodes of inflammation separated by a disease-free period. Anterior and diffuse forms of uveitis were defined as granulomatous if large keratic precipitates or iris nodules were present. Laboratory and ancillary investigations were tailored for each patient as determined by history and physical findings at presentation.[31],[32],[33] Established diagnostic criteria were used for the confirmation of the etiological diagnosis.[34],[35],[36],[37],[38] The statistical analysis was performed using Chi-square test, t -test as appropriate. Mean age of individual diagnosis was compared with overall mean age (36.5 years) by t -test to analyze the differences in the age distribution in different diagnostic entities.

The total number of outpatients attending the hospital during the study period was 11,72,258. Of 11,72,258 patients, 9378 were found to have uveitis, accounting for 0.8% of the total outpatient visits. Of 9378, the records of 8759 uveitis patients were entered in a database for the analysis, 619 patients were excluded from the study because they failed to attend the follow-up visit. Of 8759 patients, 80.1% were from Tamil Nadu state and the remaining were from Kerala (10.1%) Andhra Pradesh (7.7%), Karnataka (0.3%), North Indian states (1.3%) and 46 were from outside India (0.5%). Demographic details are given in [Table 1], mean age of the patients was 36.5 (�15.5) years (95% CI; 36.18 to 36.82 years). More than 60% of the patients were in the third to fifth decades, 7.0% of patients were 16 years of age or less and 7.3% of them were 60 years or above. Male, Female ratio of the uveitis patients (1.6:1) showed higher male predominance than the general ophthalmic patients in the same hospital (1.3:1, P P Age and gender distribution

Uveitis affects young adults most commonly. In previous clinic-based surveys, roughly 60-80% of all patients were in the third through sixth decade of life with a mean age at presentation most often between 35 and 45 years of age. [1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[39] Uveitis was reported less frequently in children and in the elderly, with children constituting approximately 5-16%[40],[41],[42],[43] and the elderly accounting for 6-21.8% of cohorts.[10],[44],[45] Similar results were obtained from our survey, where 85.6% of patients were between 17 and 59 years of age and the mean age was 36.5 years. Pediatric and elderly patients in our cohort contributed to 7% and 7.3%, respectively.

With a few exceptions,[14],[21] most uveitis surveys from developed countries report either an equal gender distribution[8],[15],[16],[17],[23] or a slight predominance of women.[5],[9],[10],[11],[19] In studies from the United States, Europe and Japan, for example, women outnumbered men by 30% to 60%.[9],[10],[11],[19] In contrast, except a few[1],[2],[3] the surveys from developing countries, including two previous reports from India[5],[11],[12],[21],[23] described a male predominance of nearly 2:1. Similar results were observed in our cohort from South India. This difference was least pronounced in patients with intermediate uveitis, a disorder known to be particularly common in women, where the M:F ratio was 1.3:1 [Table 1]. Factors contributing to such a clear male predominance in uveitis surveys reported from developing countries are undoubtedly complex. Consul and colleagues[23] have suggested that men tend to seek medical attention more often than women in agricultural societies and this may certainly have contributed to the trend in our clinic. Moreover, socioeconomic habits may put male patients at a greater risk of certain types of uveitis, particularly infectious forms such as leptospirosis[25],[26],[27],[28] and pediatric parasitic-induced granulomas,[29] which appear to affect men and boys disproportionately in South India where both disorders have been associated with exposure to contaminated water.

Primary location of inflammation

Most reports published to date have suggested that anterior uveitis is the most common form of intraocular inflammation.[1],[2],[3],[5],[6],[7],[9],[11],[13],[14],[15],[16],[17],[18],[20],[22] followed in turn by posterior, diffuse and intermediate uveitis.[7],[9],[11],[15],[18],[20] A few clinic-based surveys have, however, described diffuse[4],[8],[10] and posterior uveitis[4],[19],[21] as most common, a difference that may be attributed to referral bias, including the existence of a close collaboration with retina specialists in particular clinics. Diffuse uveitis was reported to be particularly common in Japan,[4],[10],[46] perhaps because of the high prevalence of Vogt-Koyanagi-Harada (VKH) disease, Behcet's syndrome and sarcoidosis, which often present with both anterior and posterior inflammation. Posterior and diffuse uveitis were remarkably common in reports from Africa, which could be attributed to a high incidence of infectious uveitis such as toxoplasmosis and onchocerciasis which affect mainly the posterior segment.[12],[21] A relatively low incidence of anterior uveitis in the South African population has also been assumed to be due to a low prevalence of the HLA-B27 halotype in that population.[12],[21] Anterior uveitis was the most common form of intraocular inflammation in our South Indian population, followed in turn by diffuse, post and intermediate uveitis. Biswas[11] from south India previously reported a higher frequency of posterior uveitis than diffuse, perhaps due to the relatively high frequency of toxoplasmosis and serpigenous choroiditis in their center.

Acute and chronic uveitis

Acute forms of uveitis tend to predominate in community-based hospitals[14] whereas chronic forms of uveitis tend to be more common in tertiary referral practices.[1],[9],[22] In one comparative study, for example, acute uveitis constituted 83.4% of community practices, but only 34.9% in a university practice.[14] Hence, the predominance of acute uveitis in our cohort most probably reflects the community-based care provided at present study. A higher frequency of infectious causes of anterior uveitis, such as leptospirosis and herpetic uveitis, may also have contributed to the preponderance of acute uveitis, however.

Unilateral and bilateral entities

While unilateral uveitis appears to be either equal or more common in both the developed[14],[22] and developing world,[1],[12] the etiologies in the two settings appear to differ dramatically. In the developed world the most common cause of unilateral involvement are uveitis associated with spondyloarthropathies,[4],[8],[9],[13],[14],[15],[16],[17],[18],[19],[20],[22] Fuch's heterochromic uveitis[7],[8],[9],[10],[11],[13],[15],[16],[20] and herpetic anterior uveitis.[7],[13],[14],[16],[17],[18] In contrast, the studies from the developing world, including the present report, include relatively high prevalence of traumatic uveitis,[11] herpetic[1],[2] toxoplasmosis,[23] lens-induced uveitis[5],[11],[23] parasitic pediatric anterior uveitis[29] and leptospirosis[25],[26],[27],[28] as important causes of unilateral inflammation. The bilateral uveitis is more common in some studies from the developed world[4],[9],[17] probably due to a high frequency of uveitis such as sarcoidosis[9] and Behcet's syndrome[17] which commonly affect both the eyes. While some of the bilateral entities like onchocerciasis are unique to certain geographical locations in the developing world,[47],[48],[49] the other specific bilateral entities seen in our population are VKH syndrome, sympathetic ophthalmia, serpigenous choroiditis and a proportion of leptospiral uveitis (31%).

Nongranulomatous and granulomatous uveitis

In general, nongranulomatous uveitis, which has been reported to constitute 51-89% of cases in previous series, occurs more often than granulomatous uveitis.[1],[9],[13] In the present study, 74% of our patients had nongranulomatous uveitis. The causes and frequency of common nongranulomatous uveitis varied widely in previous reports[1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23] but included uveitis associated with the sero-negative spondyloarthropathies (2-17.6%), Fuch's heterochromic uveitis (0.6-10%), traumatic uveitis (0.7- 8%), Juvenile Idiopathic Arthritis (JIA) (0.2-5.6%) and Behcet's syndrome (0.3-28%).[1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23] In contrast to previous reports, the most frequent nongranulomatous form of uveitis observed in our population was leptospirosis (9.7%). This was followed in turn by Fuch's heterochromic uveitis (4.8%), traumatic uveitis (4.4), the sero-negative spondyloarthropathies (4.1%) and Behcets syndrome (0.6%). The most common causes of granulomatous uveitis in previous studies from developed countries included sarcoidosis (0.5-18.1%), VKH disease (0.4-10%) and sympathetic ophthalmia (0.2-3.8%) while in developing countries, tuberculosis (0.2-30%)[3],[5],[11],[23] and leprosy[3],[11],[17] (0.2-1.2%) were noted in addition. The common causes of granulomatous uveitis observed in our population were tuberculosis (5.6%), sarcoidosis (4%), pediatric parasitic-induced uveitis (2.5%), VKH syndrome (1.4%), leprosy (1.2%) and sympathetic ophthalmia (0.8%). A significantly higher proportion of granulomatous uveitis was noted in children (38%) than in the middle-aged and elderly (14.8%) ( P Infectious uveitis - Developed world

Infectious uveitis accounted for relatively a minority of cases in most surveys reported from the developed world.[8],[9],[10],[14],[15],[16],[17],[18],[19],[20],[22] Toxoplasmosis was the single most common cause of infectious uveitis (3.8-17.7%) in most of these reports[5],[7],[8],[9],[13],[14],[15],[16],[17],[18],[19],[20],[22] followed by herpetic anterior uveitis[5],[6],[9],[13],[14],[16],[17],[18] (4.5-18.6%) and necrotizing herpetic retinitis[9],[13],[14],[15],[18],[19] (0.2-3.8%). Except a few,[4],[5],[7] tuberculosis[8],[9],[10],[15],[16],[17],[18],[19] and syphilis[8],[9],[14],[15],[16],[18],[19],[20],[22] appear to be rare causes of uveitis in developed countries, with a prevalence below 3%. Patients from rural areas had significantly higher frequency of infectious uveitis in a report from Poland. The explanation given by the author is significant human contact with animals and contaminated soil.[6] When we compare two reports from Japan, a more recent publication shows a marked increased frequency of systemic as well as ocular tuberculosis in Japan.[4],[10] Although minimal, a similar rise in tuberculosis is also seen in Netherlands.[15],[16]

Infectious uveitis - Developing world

Infectious uveitis occurs in greater frequency in the developing world, attributing from 11.9% to 50% of cases to infection [Table 9]. The most common infectious forms of uveitis seen in developing countries include onchocerciasis,[47],[48],[49] toxoplasmosis[1],[3],[24] herpetic uveitis[1],[6],[12] tuberculosis,[3],[23] leprosy,[23] leptospirosis[25],[26],[27],[28] and other parasitic diseases.[29],[50] Onchocerciasis is common only in certain geographical areas in South America and Africa.[46],[47],[48],[49],[50] It accounted for 50 to 60% of blindness in Nigeria and formed the third cause of bilateral blindness in the Central African Republic.[46],[47],[48],[49] Infectious uveitis accounted for 35% of uveitis in one study from the Congo, Africa and included acquired immune deficiency syndrome (AIDS) (12.5%), herpes zoster (6.4%), toxoplasmosis (6.0%), tuberculosis (6.0%) and onchocerciasis[49] (4%). Toxoplasmosis was the second most important cause of uveitis (43%) after onchocerciasis in Sierra Leone, West Africa.[12] Similarly, in Brazil,[24] a population-based household survey revealed a higher prevalence of ocular toxoplasmosis (17.7%). A study from Saudi Arabia showed 36% cases to be infectious, with the most common being herpetic anterior uveitis (16%), tuberculosis (10.5%) and toxoplasmosis (6.5%).[5] A report from China claims a lower incidence of infectious uveitis including toxoplasmosis, however, authors declare a possibility of a bias because most of the infectious uveitis cases were handled at the retina clinic and also because of some posterior uveitis were grouped under a general heading of "fundus diseases" without a specific etiology.[2] Similar to our data, Yang from China reports absence of ocular histoplasmosis.[2]

An earlier Indian study reported a remarkably high prevalence of tuberculosis (30%), toxoplasmosis (7.2%), syphilis (5.4%) and leprosy (1.2%)[23] and in a latter one[11] from south India, infectious uveitis accounted for only 11.9% of cases and the predominant infection reported was toxoplasmosis (8%) followed by tuberculosis (0.6%) and herpetic anterior uveitis 5 (0.5%). However, a more recent study from North India shows tuberculosis and toxoplasmosis to be the commonest forms of infective uveitis.[3] In our present study, infections attributed to 30.7% of uveitis, the most common infectious forms in our population were leptospiral uveitis (9.7%) followed by tuberculosis (5.6%), herpetic anterior uveitis (4.9%), pediatric parasitic-induced anterior uveitis (2.5%) and toxoplasmosis (2.5%). The prevalence and types of infectious uveitis in our cohort further differed when causes were stratified according to the age groups. Infectious uveitis was more common in children, where the most common cause was pediatric parasitic anterior uveitis (29.6%), followed in turn by endophthalmitis (8%), leptospirosis (5.5%) and toxoplasmosis (4.7%). The occurrence of pediatric parasitic anterior uveitis in children appears to be a unique feature in this population.[29],[51] In middle-aged patients, the most common infectious cause was leptospiral uveitis (10.5%) followed by tuberculosis (5.9%) and herpetic anterior uveitis (4.5%). The high frequency of leptospiral uveitis in middle-aged patients is probably related to an increased exposure to contaminated water in this working age group.[27] In older patients, the most common infectious cause of uveitis was herpetic anterior uveitis (12.1%), followed by leprosy (3.6%) and leptospirosis (3.4%). The risk and prevalence of infectious uveitis in our cohort also varied considerably by anatomical location of the inflammation, infectious uveitis was more in posterior and diffuse forms ( P Noninfectious uveitis

Epidemiological data suggest considerable variation in the frequency of noninfectious uveitis throughout the world depending upon the population studied. In general, the noninfectious uveitis syndromes are more common in developed countries, mainly because of lower prevalence rates of the various infectious forms of uveitis. Uveitis associated with the sero-negative spondyloarthropathy was the most common noninfectious entity (4-17.6%) in most of the studies,[2],[3],[4],[5],[8],[9],[11],[13],[14],[15],[16],[17],[18],[19],[20],[22] except in Japan[10] (2.5%) and Italy[7] (2.4%) where it was relatively rare. However, a more recent report from Japan[4] suggests an increased incidence of spondylopathy-associated uveitis. The second common noninfectious entity was sarcoidosis which accounted for 5-18.1% in the US, Netherlands and Japan.[4],[8],[9],[10],[13],[15],[16],[22] Sarcoidosis, however, appears to be rare in Italy[7] (0.8%), Israel[17] (0.5%), Portugal[18] (1.6%) and China (0.1%)[2]. The Behcet's syndrome is the leading cause in Turkey,[52] Saudi Arabia,[5] Israel,[17] China,[2],[53] Iran[54] and Japan[4],[10],[46] (6.5-28%) although there is a decline in the number of Behcet's in Japan in a recent report.[4] A study from North India highlights serpigenous choroidopathy as a leading cause of posterior uveitis and VKH syndrome and sympathetic ophthalmia more common non infectious panuveitis as in our present study.[3] In the present study, Fuch's heterochromic uveitis (4.8%), traumatic uveitis (4.4%), sero-negative spondyloarthropathy (4.1%) and sarcoid uveitis (4.0%) were found common, followed by lens-induced uveitis (2.0%), VKH syndrome (1.4%) and serpigenous choroidopathy (1.2%). A report from China[2] reveals a high proportion of Behcet's syndrome (16.5%), VKH syndrome (15.9%) and sympathetic ophthalmia (1.6 %) which are remarkably higher than all other reports. Like the present study, Yang from China reports absence of Bird shot retino choroidopathy in the Chinese population.[2] The prevalence of these noninfectious uveitis differed with age, however. In the literature, the commonest noninfectious uveitis in children is JIA[40],[41],[42],[43] whereas, in the elderly it appears to be sarcoidosis (8-20%) and sero-negative spondyloarthropathy[44],[45] (6-6.5%) In our population, traumatic uveitis and parsplanitis were more common in children (5.8%), whereas lens-induced uveitis (10.6%) was common in elderly patients.

We described the causes and characteristics of uveitis seen in a large, community-based eye hospital in South India. Infections accounted for nearly one-third of all cases of intraocular inflammation and included leptospiral uveitis, tuberculous uveitis and herpetic anterior uveitis. Etiologies varied with the age group of the patients. The most common cause of uveitis in children below 16 years of age was a recently described form of anterior chamber granuloma believed to result from infection by a parasite.[29],[51] The most common infectious cause in adults was leptospirosis. Leptospirosis, a zoonotic disease of global importance has been recognized as reemerging bacterial pathogens in India.[55],[56],[57],[58],[59],[60],[61],[62],[63] Probably because of the tropical climate and agricultural occupation, these differences are noted in this population.

 Conclusion



Changing patterns are seen in the studies from the same country done at different periods of time. [1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23] A few such examples are, a decreased frequency of Behcet's disease and sarcoid with an increased frequency of tuberculosis have been noted in the studies from Japan.[4],[10],[46] Also, there is an increase in the incidence of spondyloarthropathy in Japan.[4],[10],[46] Again there is an upsurge in tuberculosis and serpigenous choroidopathy in India[3],[11],[23] and there is emergence of newer entities.[25],[26],[27],[28],[29] However, as stated by BenEzra,[40] the cause for the variable incidence of specific uveitic etiologies reported in different studies is also due to a "pattern changes in uveitis diagnosis". These pattern changes are because of a multitude of factors, including genetic, ethnic, geographic and environmental factors in addition to "changing pattern of uveitis" over the years. The best examples are from Africa. The pattern is entirely different in South and North Africa, onchocerciasis is common only in certain geographical areas in South Africa. Causes of uveitis vary considerably by geographic location around the world. Awareness of such regional differences in the disease pattern is essential in deriving a region-specific list of differential diagnoses and also in understanding the predictive values of diagnostic tests which in turn facilitate the final diagnosis.

 Acknowledgments



We sincerely thank Aravind Eye Care System for financial assistance, Emmett T. Cunningham, Jr, MD, PhD, MPH for his thought-provoking discussions and suggestions offered throughout this work. We extend our sincere thanks to Mrs. Shantheeswari and Mr. Karthik Prakash for meticulous data entry and data analysis.

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