Vol. 21, No. 1 Printed in Great Britain

International Journal of Epidemiology © International Epidemiologies) Association 1992

Epidemiology of Trachoma in Bebedouro State of Sao Paulo, Brazil: Prevalence and Risk Factors EXPEDITO J A LUNA.* NORMA H MEDINA,** MARCIA B OLIVEIRA,* OSWALDO M DE BARROS,** ALEXANDRE VRANJAC,* HELOISA HELENA B MELLES.f SHEILA WESTft AND HUGH R TAYLORtt

Trachoma is still one of the most prevalent infectious diseases. It is estimated that about 500 million people are infected with trachoma and six million are blind from it. With the general improvement in living standards, trachoma has disappeared from North America, Europe, and Japan; and it is now unusual in urban communities in developing countries.' Trachoma is still common in the poorest areas of the Third World, especially in large regions of Africa, the

Middle East, and in the dry areas of southwestern Asia and the Indian subcontinent where it occurs mainly among rural communities.2 In Brazil, trachoma is thought to have arrived in the eighteenth and nineteenth centuries, and its spread is associated with European immigration in the states of Ceara, Sa"o Paulo, and Rio Grande do Sul. However, trachoma soon spread throughout the country with high prevalence rates being reported countrywide by the beginning of the twentieth century.3 Around the mid 1940s, the prevalence of trachoma began to decline, especially in the state of S3o Paulo. By the late 1960s, the State Health Department of S3o Paulo considered trachoma to have been eradicated.4 However, in 1982 new cases of inflammatory trachoma were first reported in preschool children in Bebedouro, a town in northwestern S3o Paulo (Figure 1). In 1984 and 1985 when official notification was required, 749 cases of inflammatory trachoma were reported.3 A series of investigations on the epidemiology of trachoma was undertaken in order to determine the magnitude of the problem and the risk factors associated with trachoma in this area.

•Epidemiologic Surveillance Center, Sao Paulo Health Department, Sffo Paulo, Brazil ••Sanitary Ophthalmology Service, World Health Organization Collaborating Center for the Prevention of Blindness Program, Institute of Health Sa"o Paulo State Health Department, SSb Paulo, Brazil tlnstitute Adolfo Lutz, SSb Paulo State Health Department, Sa"o Paulo, Brazil JThe Dana Center for Preventive Ophthalmology of the Wilmer Institute and The School of Public Health, The Johns Hopkins University, World Health Organization Collaborating Center for the Prevention of Blindness, Baltimore, MD, USA. Reprint requests to: Oswaldo Monteiro de Barros, Rua Itapeva, n° 300, CEP: 18400 Sfc Paulo, SP, Brazil. Sadly Dr Alexandre Vranjac has died since this paper was prepared.

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Luna E J A (Epidemiologic Surveillance Center, SSo Paulo State Health Department, S3o Paulo, Brazil), Medina N H, Oliveira M B, de Barros 0 M, Vranjac A, Melles H H B, West S and Taylor H R. Epidemiology of trachoma in Bebedouro State of SSo Paulo, Brazil: Prevalence and risk factors. International Journal of Epidemiology 1991; 20: 169-177. Trachoma was considered to have been 'eradicated' from the state of Sao Paulo, Brazil, until 1382 when a number of new cases of trachoma were reported in preschool children in Bebedouro, a small town in northwestern Ss"o Paulo. A household survey was undertaken to assess the prevalence and epidemiological characteristics of trachoma. A total of 2939 people of all ages was examined having been selected from a two-stage probalilistic household sampling frame based on census data. Overall, 7.2% of the population had evidence of one or more signs of trachoma and 2.1% had inflammatory trachoma. Inflammatory trachoma was more common in children aged one to ten years, especially in the peripheral urban and rural areas, and was more common in boys. The presence of chlamydia was confirmed by direct fluorescent antibody cytology. No cases of blindness due to trachoma were seen. A number of socioeconomic and hygiene variables were studied in order to determine the independent risk factors for trachoma in a household. Variables significantly associated with the occurrence of trachoma in the household were the number of children in the house aged one to ten years, the 'per capita' water consumption, the frequency of garbage collections, source of water, and the educational level of the head of household. Clustering of trachoma in different parts of this community was entirely explained by the concentration of households with these characteristics.

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Overview In order to determine the frequency and distribution of trachoma, a household survey was conducted in a representative sample of the population of Bebedouro. Field teams visited all households included in the sample and conducted eye examinations and interviews and collected laboratory specimens. All trachoma cases diagnosed were treated according to World Health Organization guidelines2 and referred to the regular health care unit. Field work was conducted between April and July 1986.

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ATLANTIC OCEAN FIGURE 1 Map showing study site, the town of Bebedouro in the state o/S3b Paulo, Brazil.

The clinical diagnosis of trachoma is relatively straightforward. However, in the present study it was considered important to have laboratory confirmation of the presence of the causative agent. Chlamydia trachomatis, especially as trachoma was believed not to exist in Bebedouro. The laboratory technique chosen was direct smear fluorescent antibody cytology (DFA). This technique uses monoclonal antibodies to detect the elementary bodies of C. trachomatis in specimens observed by fluorescent microscopy. In other settings DFA has given good results in terms of specificity and sensitivity:6'7 and because of its simplicity, it can be readily used in a field survey. The present paper reports the findings on the age, sex, and geographical characteristics of the prevalence of trachoma observed in Bebedouro, and the results of DFA cytology which confirm the presence of Chlamydia. Data on risk factors for imflammatory trachoma in households with children aged one to ten years are also presented. MATERIALS AND METHODS Site of Study Bebedouro is a 'municipality' (administrative division) in northwestern S2o Paulo. In 1985, its population was estimated to be 50 285, with 13.5% living in rural areas. This area is the largest producer of orange juice in Brazil and most of the land is occupied by orange plantations.

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10 PouloCity

Sample The sampling scheme reflected the need: (1) to assess the prevalence of inflammatory trachoma in children who form a high-risk age group, and (2) to determine the prevalence of any signs of trachoma, especially of scan-ing, among the population as a whole. Sample size calculations indicated that a sample of 2000 children would be sufficient to detect a prevalence of inflammatory trachoma of 5%, allowing for a confidence interval of 0.01 and a Type 1 error of 5%. The town was stratified according to estimated differences in trachoma prevalence within census sectors to ensure adequate coverage of each area and provide maximum coverage of areas with the highest rates of trachoma. This was done by using the officially reported trachoma cases collected prior to the survey and the most recent census data (1980), to calculate the rate of previously-reported trachoma cases for each census sector. The prevalence rates appeared to be higher in the outskirts of the town with decreasing prevalence closer to the centre. Similarly, the number of children aged one to ten per household was higher in the peripheral areas where the average family income was lower.8 With these data, it was possible to group the geographical sectors of Bebedouro's urban area into four strata (Figure 2). To permit an assessment of urban/rural differences, a fifth stratum with two rural villages 20 kilometres from town was added. In this study, the sample unit was the household. A probabilistic household sample was drawn in two phases. In the first phase, the sectors for study were selected with a stratum-specific, known probability in order to provide maximum coverage of the sectors with the highest rates of trachoma. The households within the selected sectors were listed and divided into two subpopulations—households with children aged one to ten years and households without children in this age group. Then a sample of households with children aged one to ten years was selected from each stratum with a probability specific for each stratum.

EPIDEMIOLOGY OF TRACHOMA IN BRAZIL



STRATUM I

Q STRATUM 2 •

STRATUM 3



STRATUM 4

Likewise, households without children were selected with a stratum-specific probability, although a different probability from that of the sample of households with children. The actual households were then selected using a random start within the stratum and a systematic selection procedure. In the following analysis, the data of the five strata were weighted appropriately in order to estimate the population prevalence, and the results are presented as adjusted prevalences. Opthalmic Examination An external eye examination was done with a binocular loupe (2.5 x). The lids and cornea were examined first; then the upper eye lid was everted and the conjunctiva covering the inner surface of the upper lid, the tarsal conjunctiva, was examined. All examinations were performed by ophthalmologists who underwent standardized training in the new World Health Organization (WHO) trachoma grading scheme as follows.9 TF - Trachomatous inflammation-Follicular TI - Trachomatous inflammation-Intense TS - Trachomatous Scarring TT - Trachomatous Trichiasis CO - Corneal Opacity In the following analysis, a case was defined by the presence of one or more of these signs, although no corneal opacities were observed in this survey. Laboratory Tests All people with trachomatous inflammation, that is the presence of either TF or Tl (TF/TI), together with their household contacts, had conjunctival scrapings collected from their right eye. Specimens were col-

lected with a Dacron swab, placed on a glass slide, air dried and fixed with acetone. In the laboratory, they were stained with 30u.l of DFA reagent (MicroTrak direct specimen reagent, Syva Inc., Palo Alto, CA)— and incubated for 30 minutes at room temperature in a moist chamber. Slides were read under a fluorescent microscope. The microscopist was unaware of the previous clinical diagnosis. The results were determined to be positive when five or more elementary bodies, characteristic of C. trachomatis, were detected in the slide.7 Risk Factors The analysis of risk factors for inflammatory trachoma was confined to households containing children aged one to ten years. A positive outcome variable was defined as a household with inflammatory trachoma in any child aged one to ten years; households with no inflammatory trachoma in the children served as controls. The households were categorized as containing none or some children with inflammatory trachoma. Data on socioeconomic status, sanitary conditions, and hygiene practices were collected at the household level. Two compound variables were constructed as follows. Socioeconomic status of the household was based on the head of the household as follows: reported occupation, type of employment, and wage level based on Singer's social classes patterns. 10 " Per person water consumption was estimated on the basis of a municipal monthly record of water consumption for each household divided by the number of people in that household. Multiple logistic regression analysis was used to assess the independent risk associated with each factor.12 An estimate of the magnitude of clustering of trachoma within the sectors was evaluated using generalized linear models (GLIM).13 RESULTS Distribution of Trachoma The study sample consisted of 1416 households and the inhabitants of 1334 households (94.7%) were examined during the study. Most of the 82 houses not included in the study were unoccupied. There were a total of 2939 eligible people of whom 2908 were examined (99%); 1959 of them were children aged one to ten years; the remaining 980 were over ten years old. Among all those examined, 129 cases of inflammatory trachoma (TF/TI), 90 cases of trachomatous-scarring (TS), and five cases of trachomatous trichiasis (TT) were diagnosed. There were no cases of corneal opacity or blindness in the sample.

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FIGURE 2 Town map of Bebedouro showing sampling strata based on census trails and frequency of reported cases of trachoma (see text for details).

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The age-specific prevalence of trachoma by sign for the entire population adjusted for the sampling scheme was determined (Figure 3). The prevalence of TF/TI) was higher in those aged one to four years and decreased thereafter, although some women aged 35 to 44 also had TF/TI. Intense inflammatory trachoma (TI) occurred only in those aged one to ten years. Trachomatous scarring was first seen in those aged five to nine years. Thereafter, the prevalence of TS tended to increase with age, reaching a peak of 13.2"% in those aged 55 to 64 years.

TABLE 1 Estimated prevalence data weighted by sampling strata of trachoma by age and sex, Bebedouro, S8~o Paulo, Brazil, 1986 Age (ft) 1-10 years Males Females

Trachoma*

Total

> 10 years Males Females

TF TI TS TT

6.8 1.3 1.1 -

3.4 1.7 1.1 -

1.4 5.8 0.5

0.9 _ 5.1 0.6

1.8 0.3 4.7 0.4

Total

9.2

6.2

7.7

6.6

7.2

•See text for definitions

n

10

10

20

30

40

50

60

FIGURE 3 Age-specific prevalence of trachoma* by sign. •See text for definitions.

Trachomatous trichiasis occurred only in older age groups, beginning in those aged 40 to 50 years. These people are at high risk of developing corneal blindness. The total adjusted prevalence rate of any-sign trachoma was 7.2%; 2.1% of the population had inflammatory trachoma (TF/TI). The prevalence of intense inflammatory trachoma (TI) with or without TF was 0.3% while the prevalence of TS was 4.7%. The prevalence of trichiasis (TT) was low (0.4%). Overall, the prevalence of trachoma was somewhat higher in males for both age groups (Table 1). Among children aged one to ten years, boys had twice the prevalence of TF, although the prevalence of TI was slightly higher in girls. For the adults, the prevalence was higher in males in all age groups except the 30 to 39 year-old group where the prevalence was higher in women. The prevalence of trachoma in children and adults was examined in each sampling strata (Figure 4). Although the rates of TS in adults were comparable in strata 2, 3, 4 and 5, there was a progressive increase in the prevalence of active (TF/TI) in children as one moved from the central stratum 1 to the peripheral urban stratum 4 and rural stratum 5. The high pre-

n I

i 2

3

4

I -10 YEARS

5

1

2

3

4

5

OVER 10 YEARS

FIGURE 4 Prevalence of trachoma' by signs and age groups by stratum. •See text for definitions.

valence for TF in stratum 5 was somewhat surprising because prior to the survey cases had not been reported from this area.5 With a prevalence rate for TF of 18.6% in this stratum, one might have expected to see cases of severe trachoma (TI) among children, but this was not seen. In stratum 1, there were no cases of TI in those aged one to ten nor TF/TI among those over ten years. The prevalence of TS was also lowest, and there were no cases of TT. The simple association of trachoma with household variables is summarized in Table 2. Households with many children and in which the children slept together appeared to be associated with trachoma. Several measures of water utilization and sanitation were also associated with trachoma in the household. Measures of low socioeconomic status were more frequent in households with trachoma present.

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• TF •TI • TS

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INTERNATIONAL JOURNAL OF EPIDEMIOLOGY TABLE 2 Risk factors for TF/TI* in households with children aged one to ten years, Bebedouro-SSo Paulo Brazil, 1986 Risk factor

Number children 1-10 years 1 2 >3 Number of children sharing beds Sleeps alone

Number of towels per person 1 m i n i m u m wage •See text for definition

21/570(3.7) x 2 = 27/412 (6.5) (2) 36/184 (19.6)

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Epidemiology of trachoma in Bebedouro State of São Paulo, Brazil: prevalence and risk factors.

Trachoma was considered to have been 'eradicated' from the state of São Paulo, Brazil, until 1982 when a number of new cases of trachoma were reported...
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