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Review Article

Global variation and pattern changes in epidemiology of uveitis

Rathinam, S R MNAMS; Namperumalsamy, P MS, FAMS

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Indian Journal of Ophthalmology: May–Jun 2007 - Volume 55 - Issue 3 - p 173-183
doi: 10.4103/0301-4738.31936
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Abstract

Uveitis includes a large group of diverse inflammatory diseases, the frequencies of which vary considerably by geographic location around the world.1234567891011121314151617181920212223 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.682425 Among the environmental factors, the most important appears to be the regional distribution of various pathogens,242526272829 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.1234567891011121314151617181920212223

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.313233 Established diagnostic criteria were used for the confirmation of the etiological diagnosis.3435363738 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) byt -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 < 0.05) seen in the same period of time.

Table 1
Table 1:
Demographic characteristics

Anterior uveitis was the commonest form of all uveitic entities (57.4%) followed by diffuse uveitis (22.4%), posterior uveitis (10.6%) and intermediate uveitis (9.5%) [Table 2]. On the basis of overall clinical presentation, acute, unilateral and nongranulomatous forms occurred more frequently. However, acute presentation was more common in anterior and diffuse uveitis than intermediate and posterior uveitis, unilateral presentation was more common in anterior uveitis than in other types. Idiopathic uveitis constituted 44.6% of 8759 patients, followed by infectious (30.5%) and noninfectious etiologies (24.9%). Of 3909 (44.6%) idiopathic uveitis, 2246 (25.6%) were idiopathic anterior, 681 (7.8%) idiopathic intermediate, 339 (3.8%) idiopathic posterior and 643 (7.3%) idiopathic diffuse uveitis. Idiopathic entities were common in all age groups.

Table 2
Table 2:
Clinical characteristics

Etiological classifications in different age groups are given in [Table 3]. Of 8759 patients, the predominant infectious uveitis included leptospirosis (9.7%), tuberculosis (5.6%) and herpetic disorders (4.9%). Noninfectious entities comprised Fuch's heterochoromic uveitis (4.8%), traumatic uveitis (4.4%), spondyloarthropathy (4.1%), sarcoidosis (4.0%) and lens protein uveitis (2.0%). Diagnoses were stratified according to the age groups and the results of the comparison of ages of individual diagnosis with the overall mean age (36.5 years) is given in [Tables 3-7]. Juvenile idiopathic arthritis, pediatric parasitic anterior uveitis, toxoplasmosis, endophthalmitis and leptospirosis occurred in the younger population while lens-induced uveitis, leprosy uveitis, sympathetic ophthalmia, herpetic anterior uveitis and sarcoidosis were more common in the elderly population (P < 0.001).

Table 3
Table 3:
Etiological classification by age group distribution
Table 4
Table 4:
Causes of anterior uveitis
Table 5
Table 5:
Causes of intermediate uveitis
Table 6
Table 6:
Causes of posterior uveitis
Table 7
Table 7:
Causes of diffuse uveitis

The etiological subtypes in different anatomical locations are given in [Tables 4-7]. In the anterior uveitis, pediatric parasitic anterior chamber granuloma (49.3%) and traumatic uveitis (9.8%) were predominant in the pediatric age group. While herpetic anterior uveitis (16.7%), lens-induced uveitis (14.6%) and leprosy uveitis (4.9%) were found more common in the elderly population. Fuch's heterochromic uveitis (9.8%), uveitis associated with spondyloarthropathy (8.2%), herpetic uveitis, (8.2%) and traumatic (7.8%) were equally common in middle-aged patients. Table 5 shows the distribution of intermediate uveitis. Causes were unknown in the majority of intermediate uveitis uniformly in all age groups.

Toxoplasmosis (23.5%) was the most common posterior uveitis entity in all the patients irrespective of the age group. Tuberculosis was the next common cause in children (10.4%) and in middle-aged patients (13.6%). Serpigenous choroiditis and sarcoidosis predominated in elderly patients (8%) [Table 6]. The common diffuse uveitis Table 7 was endophthalmitis in the pediatric population (38.6%), leptospiral uveitis (29.7%) in middle age, leptospirosis, endophthalmitis and sympathetic ophthalmia (13.9%) in the elderly.

Uveitis-Literature Review

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.123456789101112131415161718192021222339 Uveitis was reported less frequently in children and in the elderly, with children constituting approximately 5-16%40414243 and the elderly accounting for 6-21.8% of cohorts.104445 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,1421 most uveitis surveys from developed countries report either an equal gender distribution815161723 or a slight predominance of women.59101119 In studies from the United States, Europe and Japan, for example, women outnumbered men by 30% to 60%.9101119 In contrast, except a few123 the surveys from developing countries, including two previous reports from India511122123 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 colleagues23 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 leptospirosis25262728 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.1235679111314151617182022 followed in turn by posterior, diffuse and intermediate uveitis.7911151820 A few clinic-based surveys have, however, described diffuse4810 and posterior uveitis41921 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,41046 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.1221 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.1221 Anterior uveitis was the most common form of intraocular inflammation in our South Indian population, followed in turn by diffuse, post and intermediate uveitis. Biswas11 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 hospitals14 whereas chronic forms of uveitis tend to be more common in tertiary referral practices.1922 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 developed1422 and developing world,112 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,489131415161718192022 Fuch's heterochromic uveitis789101113151620 and herpetic anterior uveitis.71314161718 In contrast, the studies from the developing world, including the present report, include relatively high prevalence of traumatic uveitis,11 herpetic12 toxoplasmosis,23 lens-induced uveitis51123 parasitic pediatric anterior uveitis29 and leptospirosis25262728 as important causes of unilateral inflammation. The bilateral uveitis is more common in some studies from the developed world4917 probably due to a high frequency of uveitis such as sarcoidosis9 and Behcet's syndrome17 which commonly affect both the eyes. While some of the bilateral entities like onchocerciasis are unique to certain geographical locations in the developing world,474849 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.1913 In the present study, 74% of our patients had nongranulomatous uveitis. The causes and frequency of common nongranulomatous uveitis varied widely in previous reports1234567891011121314151617181920212223 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%).1234567891011121314151617181920212223 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%)351123 and leprosy31117 (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 < 0.001). This was mainly due to a higher prevalence of pediatric parasitic-induced uveitis (29.6%) in the pediatric subgroup.

Etiology of Uveitis-Idiopathic Forms

For a sizable proportion of patients, the cause of uveitis remains unknown despite appropriate investigation, regardless of age, gender or anatomical location. Previous surveys have suggested that the cause of uveitis remains unknown in approximately 30-60% of patients1234567891011121314151617181920212223 [Table 8]. In general, anterior and intermediate uveitis is more often idiopathic than are posterior and diffuse forms of inflammation, and uveitis tends more often to be idiopathic in women as compared to men. In the present study, 44.6% of the total uveitis cohort and 47.8% of women had idiopathic uveitis.

Table 8
Table 8:
Demographic and onset characteristics of uveitis from different countries

Infectious uveitis - Developed world

Infectious uveitis accounted for relatively a minority of cases in most surveys reported from the developed world.89101415161718192022 Toxoplasmosis was the single most common cause of infectious uveitis (3.8-17.7%) in most of these reports5789131415161718192022 followed by herpetic anterior uveitis5691314161718 (4.5-18.6%) and necrotizing herpetic retinitis91314151819 (0.2-3.8%). Except a few,457 tuberculosis89101516171819 and syphilis8914151618192022 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.410 Although minimal, a similar rise in tuberculosis is also seen in Netherlands.1516

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,474849 toxoplasmosis1324 herpetic uveitis1612 tuberculosis,323 leprosy,23 leptospirosis25262728 and other parasitic diseases.2950 Onchocerciasis is common only in certain geographical areas in South America and Africa.4647484950 It accounted for 50 to 60% of blindness in Nigeria and formed the third cause of bilateral blindness in the Central African Republic.46474849 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 onchocerciasis49 (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

Table 9
Table 9:
Distribution of various etiologies of uveitis from different countries

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 one11 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.2951 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 < 0.005) than in anterior and intermediate forms in adults. However, herpetic uveitis and pediatric parasitic uveitis was the most frequent infectious anterior uveitis. As in several previous studies12345678910111213141516171819202223 toxoplasmosis was the most common posterior uveitis in our population as well, irrespective of age and gender. Leptospirosis was the predominant cause of diffuse uveitis.

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,23458911131415161718192022 except in Japan10 (2.5%) and Italy7 (2.4%) where it was relatively rare. However, a more recent report from Japan4 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.4891013151622 Sarcoidosis, however, appears to be rare in Italy7 (0.8%), Israel17 (0.5%), Portugal18 (1.6%) and China (0.1%)2. The Behcet's syndrome is the leading cause in Turkey,52 Saudi Arabia,5 Israel,17 China,253 Iran54 and Japan41046 (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 China2 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 JIA40414243 whereas, in the elderly it appears to be sarcoidosis (8-20%) and sero-negative spondyloarthropathy4445 (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.2951 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.555657585960616263 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.1234567891011121314151617181920212223 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.41046 Also, there is an increase in the incidence of spondyloarthropathy in Japan.41046 Again there is an upsurge in tuberculosis and serpigenous choroidopathy in India31123 and there is emergence of newer entities.2526272829 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.

Source of Support:

Aravind Eye care System.

Conflict of Interest:

None declared.

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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Keywords:

Epidemiology; tropical country; uveitis

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