Abstract

INTRODUCTION

Trachoma, an inflammatory disease of the eye affecting the cornea and conjunctiva, the evolution of which involves chronic relapse, is caused by Chlamydia trachomatis serotypes A, B, Ba and C and is the main cause of preventable blindness in the world. The World Health Organization (WHO) estimates that there are 41 million individuals, worldwide, with active trachoma and 7.6 million with trichiasis, the clinical sequelae of the disease, while 1.3 million suffer serious visual impairment and blindness.⁹9. Mariotti SP, Pascolini D, Rose-Nussbaumer J. Trachoma: global magnitude of a preventable cause of blindness. Br J Ophthalmol. 2009;93(5):563-8. DOI:10.1136/bjo.2008
https://doi.org/10.1136/bjo.2008... ^{, 13}13. Resnikoff S, Pascolini D, Etya'ale D, Kocur I, Pararajasegaram R, Pokharel GP, et al. Global data on visual impairment in the year 2002. Bull World Health Organ. 2004;82(11): 844-51. DOI:10.1590/S0042-96862004001100009
https://doi.org/10.1590/S0042-9686200400... Trachoma is linked to poor socioeconomic conditions and poor sanitation and hygiene.

In Brazil, trachoma was considered a significant health problem until the first half of the 20^th century. Prevalence in the country then declined markedly from the 1960s onwards. The Ministry of Health carried out a national survey in 1974-1976 and, concluding that trachoma had been eradicated in some regions and was at sub-endemic level in others, prioritized work in specific areas, so-called "endemic pockets", in which prevalence reached 30%.⁴4. Freitas CA. Bolsões hiperendêmicos de tracoma: situação atual. Rev Bras Malariol Doenças Trop. 1977;29:33-76. However, various studies realized after the mid 1980s, in different regions and states, found prevalence varying between 1.5% and 47.7% for active trachoma and from 0.1% to 2.0% for trichiasis, including indigenous populations.¹1. Alves APX, Medina NH, Cruz, AAV. Trachoma and ethnic diversity in the upper Rio Negro Basin of Amazonas State, Brazil. Ophthalmic Epidemiol. 2002;9(1):29-34. DOI:10.1076/opep.9.1.29.1716
https://doi.org/10.1076/opep.9.1.29.1716... ^{, 2}2. Caligaris LSA, Morimoto WTM, Medina NH, Waldman EA. Trachoma prevalence and risk factors among preschool children in a central area of the city of São Paulo, Brazil. Ophthalmic Epidemiol. 2006;13(6):365-70. DOI:10.1080/09286580601013078
https://doi.org/10.1080/0928658060101307... ^{, 5}5. Koizumi IK, Medina NH, D'Amaral RKK, Morimoto WTM, Caligaris LSA, Chinen N, et al. Prevalência de tracoma em pré-escolares e escolares no Município de São Paulo. Rev Saude Publica. 2005;39(6):937-42. DOI:10.1590/S0034-89102005000600011
https://doi.org/10.1590/S0034-8910200500...

6. Lucena AR, Cruz AAV, Cavalcanti R. Estudo epidemiológico do tracoma em uma comunidade da Chapada do Araripe - Pernambuco - Brasil. Arq Bras Oftalmol. 2004;67(2):197-200. DOI:10.1590/S0004-27492004000200003
https://doi.org/10.1590/S0004-2749200400...

7. Luna EJA, Medina NH, Oliveira MB. Vigilância epidemiológica do tracoma no Estado de São Paulo. Arq Bras Oftalmol. 1987;50(2):70-9. ^{- 8}8. Luna EJA, Medina NH, Oliveira MB, Barros OM, Vranjac A, Melles HH. Epidemiology of trachoma in Bebedouro, State of São Paulo, Brazil: prevalence and risk factors. Int J Epidemiol. 1992;21(1):169-77. DOI:10.1093/ije/21.1.169
https://doi.org/10.1093/ije/21.1.169... ^{, 11}11. Medina NH, Gentil RM, Oliveira MB, Sartori MF, Cabral JH, Vasconcelos MS, et al. Investigação epidemiológica do tracoma em pré-escolares e escolares nos municípios de Franco da Rocha e Francisco Morato - São Paulo, 1989. Arq Bras Oftalmol. 1994;57(3):154-8. ^{, 12}12. Paula JS, Medina NH, Cruz AAV. Trachoma among the Yanomami Indians. Braz J Med Biol Res. 2002;35(10):1153-7. DOI:10.1590/S0100-879X2002001000007
https://doi.org/10.1590/S0100-879X200200... ^{, 14}14. Scarpi MJ, Plut RCA, Arruda HO. Prevalência do tracoma no povoado de Mocambo, Estado do Ceará, Brasil. Arq Bras Oftalmol. 1989;52(5):177-9. ^{, 15}15. Scarpi MJ, Silva RJM, Ferreira IA, Barbosa FAC, Plut RCA. Prevalência de tracoma em bairro do município de Palmares, Estado de Pernambuco, Brasil. Arq Bras Oftalmol. 1990; 53(4):171-4.

The WHO considers trachoma to be a neglected disease. According to its criteria for eliminating the disease as a cause of blindness, the prevalence of trachomatous inflammation - follicular needs to be reduced to under 5% in children aged from one to nine, and prevalence of trachomatous trichiasis to less than one case per thousand inhabitants in a community or district.^aaWorld Health Organization. Report of the 2nd Global Scientific Meeting on Trachoma; 2003 Aug 25-27; Geneva. (WHO/PBD/GET/03.1).

In 1997 the Alliance for the Global Elimination of Blinding Trachoma by 2020 was created, under WHO leadership.^bb World Health Organization. Planning for the Global Elimination of Trachoma (GET): report of a WHO Consultation. Geneva; 1997. Brazil has participated in this initiative from the start and the Ministry of Health has reiterated its adherence to the goals of elimination. Thus, in order to support actions to control it, a national survey was carried out to discover the prevalence and distribution of the disease among schoolchildren, as there are no up to date national data.

The aim of this study was to estimate the prevalence and describe the distribution of trachoma among Brazilian schoolchildren in municipalities with a Human Development Index - Municipal below the national average.

METHODS

A cross-sectional study was carried out with pupils from the first to fourth year of primary education, attending public schools in municipalities a Human Development Index - Municipal below the national average, and in the Distrito Federal (DF). The municipalities were chosen based on the knowledge that trachoma is more prevalent in poorer communities,⁹9. Mariotti SP, Pascolini D, Rose-Nussbaumer J. Trachoma: global magnitude of a preventable cause of blindness. Br J Ophthalmol. 2009;93(5):563-8. DOI:10.1136/bjo.2008
https://doi.org/10.1136/bjo.2008... thus allowing the investigation to be more focused.

There was no age limit for the participants, any pupil attending the year groups in question being deemed eligible.

The survey was carried out between 2002 and 2007, using probabilistic sampling selected through a procedure of stratified cluster sampling.

The sample size was calculated considering a 5% prevalence of active trachoma, accepting a maximum sampling error of 1% in 95% of the possible samples. An additional 20% was added to compensate for losses, giving an estimated sample of 2,400 pupils. This number was then multiplied by three, as three strata were created, resulting in a total of 7,200 pupils for each state.

The municipalities of each state, with HDI-M below the nation mean, were stratified according to population (Demographic Census 2000), using terciles as cutoff points, constituting three population strata, namely: small, medium and large municipalities.

For each population strata, a list of all the public schools and their respective number of pupils in first to fifth grade was composed and ordered according to municipality and location of the school (urban or rural).^ff Ministério da Educação. Censo Escolar da 1ª a 4ª série do ensino fundamental, disponibilizados nos anos 2001-2006. Next, a systematic sample was selected from each list so that the proportional distribution of schools according to municipality and location (urban or rural) was similar to that of the population strata. All of the pupils registered in the schools were included in the sample.

For the purposes of this study, the administrative regions corresponding to the satellite cities in Brasília, DF, Midwestern Brazil, were considered to be municipalities. In the period in which the survey was carried out, the DF was constituted of 19 administrative regions, of which only two had HDI-M below the national mean.^cc Programa das Nações Unidas para o Desenvolvimento; Instituto de Pesquisa Econômica Aplicada; Fundação João Pinheiro. Atlas do Desenvolvimento Humano no Brasil. Brasília (DF); 1998 [cited 2013 Jun 26]. Available from: http://www.pnud.org.br/IDH/Atlas1998.aspx?indiceAccordion=1&li=li_Atlas1998 Consequently, only one population strata was considered and, thus, the sample for the DF was 2,400 schoolchildren.

In this study, results of the survey carried out in the following states are presented: Acre, Alagoas, Bahia, Ceará, Distrito Federal, Goiás, Maranhão, Minas Gerais, Mato Grosso do Sul, Pará, Paraíba, Piauí, Rio Grande do Norte, Rio Grande do Sul, Roraima, Santa Catarina, Sergipe, São Paulo and Tocantins. The 3,484 municipalities with HDI-M below the national mean in these states had a population of 70,831,574 inhabitants, 122,833 public schools with 10,799,725 school children registered.

Two cut off values for the HDI-M were used due to the availability of information on HDI-M at the start of the study and its being updated after 2000 (0.724 in 1991 and 0.764 in 2000).^eeCompanhia de Planejamento do Distrito Federal - CODEPLAN. Brasília (DF); 2003 [cited 2013 Jun 26]. Available from: http://www.codeplan.df.gov.br/images/CODEPLAN/PDF/Pesquisas%20Socioecon%C3%B4micas/idh.pdf

Standardized external eye examinations using a magnifying glass (2.5X) in natural or artificial light were carried out by trained examiners. All of the selected schoolchildren were examined for signs of trachoma, according to WHO criteria:¹⁸18. Thylefors B, Dawson CR, Jones BR, West SK, Taylor HR. A simple system for the assessment of trachoma and its complications. Bull World Health Organ. 1987;65(4):477-83.

The schoolchildren examined and the cases of trachoma detected were recorded on the appropriate forms and dealt with according to Ministry of Health norms.^gg Ministério da Saúde, Fundação Nacional de Saúde. Manual de controle do tracoma. Brasília (DF); 2001. ^{, h}h Ministério da Saúde, Secretaria de Vigilância em Saúde. Portaria Nº 67, de 22 de dezembro de 2005. Inclui Azitromicina no tratamento sistêmico de tracoma. Diario Oficial Uniao. 23 dez 2005. Seção I:127. Family contacts were examined and treated when trachoma was found. Analysis of the data considered the category "inflammatory trachoma or active trachoma", formed by the joining of the clinically active forms of the disease: trachomatous inflammation - follicular and intense.

The variables analyzed were: presence of clinical signs of trachoma, age, sex and location of residence (state, municipality and rural or urban zone).

The prevalence of active trachoma was estimated for each state, referring to municipalities with HDI-M lower than the national mean, with the respective 95% confidence intervals according to sex, age group, urban or rural zone and clinical form. The estimates of prevalence were corrected for design effect and weighted according to the size of the school population of the eligible municipalities of each state.

To compare the categorical variables, the Chi-squared and Chi-squared for linear trend tests were used. Spatial-geographical distribution of the prevalence of trachoma was described for municipalities and state. The EpiInfo, version 6.4 and SPSS, version 12 applications were used to analyze the data.

Thus, 119,531 schoolchildren were examined, corresponding to 90.6% of the estimated sample of 132,000 pupils, distributed throughout 2,270 schools located in 1,156 municipalities. Losses (7.6%) occurred due to children being off school on the day of the eye exam and the parents or the child themselves refusing to take part. The state with the highest rate of losses was Alagoas (16.1%) and that with the lowest rate was Acre (0.3%). No differences were observed between the actually examined sample and the losses, in relation to distribution between rural and urban zones, nor in distribution according to sex and mean and median age. Moreover, it was noted that some schools sampled had a lower number of pupils than was recorded in the Ministry of Education (MEC) School Censusf, which explains the remaining difference between the estimated sample and the sample actually examined.

The research was approved by the Ethics Committee of the Instituto Adolpho Lutz, State Department of Health, Sao Paulo, in 5^th April 2002.

RESULTS

Table 1 shows a description of the states in relation to the total number of municipalities, number of municipalities with HDI-M below the national mean and the number of schools and schoolchildren in these municipalities. According to the location of the school, 69.4% were in rural areas, although only 35.8% of total schoolchildren studied in one of these schools. In the states of Ceará and Maranhão the percentage of schoolchildren in the rural area was higher than in the urban area.

Of the total number of schoolchildren examined, 63,300 (53.0%) were male. The mean age of the sample was 9.4 years old, with a median of nine years old (maximum and minimum values were 19 and four years old, respectively). The age group from five to nine years old was the most common (58.4%), followed by the age groups from ten to 14 (38.7%), 15 and over (2.7) and from zero to four years old (0.2%). The latter is made up of a population below school age, but which regularly attended the year groups participating in this sample.

There were 6,030 cases of trachoma, both active and scarring forms, detected. Of these, 98.8% presented the trachomatous inflammation - follicular clinical form, 0.03% trachomatous inflammation - intense and 0.05% trachomatous scarring. No cases of trachomatous trichiasis or corneal opacity were detected in the sample studied (Table 2).

The 5,968 diagnosed cases of active trachoma resulted in an estimated prevalence of 5.0% (95%CI 4.6;5.4) for the municipalities with HDI-M below the national mean in the 18 states studied and the DF.

Schoolchildren in 1,156 municipalities were examined, corresponding to approximately 21% of the municipalities in Brazil, with cases of trachoma being detected in 901 municipalities (77.9%). Of the total municipalities studied, 431 (37.3%) had schools with a prevalence of trachoma > 5% and, in 255 (22.1%) of the municipalities there were no cases of trachoma detected in the schools visited (Table 3). The highest rates of prevalence were found in the states of Ceará and Acre and the lowest in the Distrito Federal and Mato Grosso do Sul (Table 4).

Table 5 shows the prevalence of active trachoma according to sex, age and location of the school. There was no difference between sex (p = 0.699). The prevalence of trachoma decreased with age (under 5s: 8.2%; five to nine years old: 5.3% ten to 14 years old: 4.6%; 15 and over: 3.6%; p < 0.01). A total of 3.196 (4.3%) cases of active trachoma occur in urban areas and 2.772 (6.2%) in rural areas (p < 0.01).

DISCUSSION

Cases of trachoma were detected in all regions, contradicting the belief that it was under control in the South and South East of the country. Trachoma still occurs more frequently in populations in rural areas, concurring with national and international literature.³3. Freitas CA. Prevalência do tracoma no Brasil. Rev Bras Malariol Doenças Trop. 1976;28:227-80. ^{, 4}4. Freitas CA. Bolsões hiperendêmicos de tracoma: situação atual. Rev Bras Malariol Doenças Trop. 1977;29:33-76. ^{, 8}8. Luna EJA, Medina NH, Oliveira MB, Barros OM, Vranjac A, Melles HH. Epidemiology of trachoma in Bebedouro, State of São Paulo, Brazil: prevalence and risk factors. Int J Epidemiol. 1992;21(1):169-77. DOI:10.1093/ije/21.1.169
https://doi.org/10.1093/ije/21.1.169... ^{, 19}19. Vieira J BF, Coelho GE. Tracoma: aspectos epidemiológicos e de controle. Rev Bras Med Trop. 1998;31(Supl 2):121-3.There was no difference with regards to the distribution of cases by sex, which is consistent with data reported in Brazilian studies of schoolchildren.¹1. Alves APX, Medina NH, Cruz, AAV. Trachoma and ethnic diversity in the upper Rio Negro Basin of Amazonas State, Brazil. Ophthalmic Epidemiol. 2002;9(1):29-34. DOI:10.1076/opep.9.1.29.1716
https://doi.org/10.1076/opep.9.1.29.1716... ^{, 2}2. Caligaris LSA, Morimoto WTM, Medina NH, Waldman EA. Trachoma prevalence and risk factors among preschool children in a central area of the city of São Paulo, Brazil. Ophthalmic Epidemiol. 2006;13(6):365-70. DOI:10.1080/09286580601013078
https://doi.org/10.1080/0928658060101307... ^{, 5}5. Koizumi IK, Medina NH, D'Amaral RKK, Morimoto WTM, Caligaris LSA, Chinen N, et al. Prevalência de tracoma em pré-escolares e escolares no Município de São Paulo. Rev Saude Publica. 2005;39(6):937-42. DOI:10.1590/S0034-89102005000600011
https://doi.org/10.1590/S0034-8910200500... ^{, 10}10. Medina NH, Oliveira MB, Tobin S, Kiil Jr G, Mendonça MM, Barros OM, et al. The prevalence of trachoma in preschool and school children in Olimpia, Guaraci and Cajobi, São Paulo, Brazil. Trop Med Parasitolol. 1992;43(2):121-3. ^{, 11}11. Medina NH, Gentil RM, Oliveira MB, Sartori MF, Cabral JH, Vasconcelos MS, et al. Investigação epidemiológica do tracoma em pré-escolares e escolares nos municípios de Franco da Rocha e Francisco Morato - São Paulo, 1989. Arq Bras Oftalmol. 1994;57(3):154-8.Distribution according to sex in Brazil differs from other countries, where higher prevalence among females has been observed.¹⁶16. Taylor HR, Velasco FM, Sommer A. The ecology of trachoma: an epidemiological study in Southern Mexico. Bull World Health Organ. 1985;63(3):559-67.

In this study, the schoolchildren's eye examinations were carried out over a mean period of two months in each state. Difficulties were encountered travelling in areas which were difficult to reach and a smaller number of pupils were registered by the Ministry of Education (MEC) Censusf especially in schools in rural areas. In spite of the large distances and logistical difficulties in some areas, the sample coverage was satisfactory and the losses deemed to be low. Therefore, the results of this study are valid and can be extrapolated to other municipalities with HDI-M lower than the national average.

The World Health Organization the disease to be under control when the prevalence of active trachoma is less than 5% in children aged between one and nine years old.ⁱi World Health Organization. Primary health care level management of trachoma. Geneva; 1989. However, rates of prevalence equal to or higher than 5% were found in various states and in all regions, indicating the need to maintain a program to control trachoma in Brazil.

The majority of positive cases found were of active trachoma, as the sample was composed primarily of children and adolescents. The data concur with those presented in the literature, as the scarring form of the disease is more commonly found in adults and in populations over the age of 60.⁴4. Freitas CA. Bolsões hiperendêmicos de tracoma: situação atual. Rev Bras Malariol Doenças Trop. 1977;29:33-76. ^{, 16}16. Taylor HR, Velasco FM, Sommer A. The ecology of trachoma: an epidemiological study in Southern Mexico. Bull World Health Organ. 1985;63(3):559-67.The expected rates of prevalence of the active forms might have been higher if the sample had included pre-school children, as they are recognized to be the main reservoir of the etiologic agent in populations where trachoma is endemic. In spite of this possible limitation, the rates of prevalence found are enough to characterize the persistence of active trachoma at levels of medium to high endemicity in a large proportion of the municipalities in Brazil.

Another possible limitation of the study would be the use of a definition of the case based on clinical criteria. This definition would be highly sensitive, but the positive predictive value (PPV) would fall as prevalence became lower. In fact, a lower PPV in the group of municipalities with very low prevalence should be considered when interpreting the results of the survey. However, only 25.3% of the municipalities had a rate of prevalence below 1%. Apart from trachoma, there are no other forms of follicular conjunctivitis which occur in an endemic form. In addition, adopting criteria for diagnosing trachomatous inflammation - follicular, which requires the presence of at least five follicles of 0.5mm in diameter in the upper tarsal conjunctiva, leads not only to the exclusion of other types of conjunctivitis which are characterized by smaller follicles, or those located outside of the upper tarsal conjunctiva, but also a lack of sensitivity, as cases of trachoma which are in the initial stage or in the process of resolution may have fewer than five follicles or of a smaller diameter.

This study did not enable the situation of the clinical sequelae of trachoma in the country to be analyzed. The most common clinical form of the disease was the least serious form. However, a significant proportion of the municipalities had a prevalence sufficiently high to maintain the risk of trachomatous scarring evolving if activities of monitoring and surveillance of trachoma are not implemented, in conjunction with inter-sectoral actions promoting health and improvements in socio-economic conditions and educating the populations.

The municipalities with municipal human development indices above the national mean were not included in this study. However, most of these studies have pockets of poverty, with populations who live in conditions of risk of suffering trachoma. It is recommended to develop and carry out surveys of the prevalence of trachoma in the municipalities with HDI-M above the national mean, in order to discover the epidemiological reality and the progress towards achieving the goals of eliminating trachoma causing blindness, recommended by the WHO.

Trachoma is a chronic disease and changes in the epidemic profile depend not only on specific interventions of prevention and control, but also on policies of developing and improving the living and health care conditions of the majority of the populations. Thus, in spite of the period of the study covering the years 2002 to 2007, it is postulated that the possible changes in living conditions in progress during this period had not yet affected the prevalence indicators. The increasing coverage of social programs aimed at reducing poverty and inequality should have an impact on the prevalence of trachoma, although this effect will only be observable in the mid to long term. The reduction in the prevalence of trachoma is linked to improvements in living conditions, sanitation and personal hygiene practices, which will follow from increasing income. Thus, the results of this study will serve as a baseline for evaluating the possible effects of interventions aimed at reducing poverty.

The occurrence of high rates of prevalence of trachoma in rural areas shows the need for more interventions aimed at improving living and health care conditions for the country's rural population. However, it should be considered that, due to the accelerate process of urbanization which has taken place over the last four decades, more than 70% of the population of Brazil live in areas considered to be urban, requiring the development of studies with a new view of the epidemiology of the disease for the peripheries of large and medium sized cities and the adoption of policies which include exclusion and different levels of access to health care services, place in which trachoma continues to occur in the poorest populations. The existence of trachoma in a population is an indicator of precarious living and health care conditions.

There are few national data available on the prevalence of trachoma in emerging countries, which makes it difficult to compare the results found in this study. The reports which exist refer to regions or to subgroups of specific age groups. The rates of prevalence found in the literature varied from 36.6% in the Nile Delta in Egypt to 60% in hyper-endemic communities in Tanzania.²⁰20. West SK, Munoz B, Mkocha H, Gayds CA, Quinn TC. Number of years of annual mass treatment with azithromycin needed to control trachoma in hyperendemic communities in Tanzania. J Infect Dis. 2011;204(2):268-73. DOI:10.1093/infdis/jir257
https://doi.org/10.1093/infdis/jir257... In Australia, prevalence of between 0.6% and 7.3% were found in Aborigines between five and 15 years old and in Mexico, in Chiapas, the estimated prevalence of trachomatous inflammation - intense was 25% in children under ten.¹⁶16. Taylor HR, Velasco FM, Sommer A. The ecology of trachoma: an epidemiological study in Southern Mexico. Bull World Health Organ. 1985;63(3):559-67. ^{, 17}17. Taylor HR, Fox SS, Xie J, Dunn RA, Arnold ALMR, Keeffe JE. The prevalence of trachoma in Australia: the National Indigenous Eye Health Survey. Med J Aust. 2010;192(5): 248-53.

In conclusion, this study shows that trachoma is still a significant health problem in Brazil, with municipalities with medium and high rates of prevalence. The data shown can be a reference in drawing up national and state plans for eliminating trachoma as a cause of blindness by 2020, as recommended in the World Health Organization directive.^aaWorld Health Organization. Report of the 2nd Global Scientific Meeting on Trachoma; 2003 Aug 25-27; Geneva. (WHO/PBD/GET/03.1).

References

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