Mapping of Wuchereria bancrofti infection in children and adolescents in an endemic area of Brazil

Acta Tropica 120 (2011) 151–154

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Mapping of Wuchereria bancrofti infection in children and adolescents in an endemic area of Brazil Eduardo Brandão a,b,∗ , Cristine Bonfim c , Danielle Cabral a , José Lancart Lima d , Ana Maria Aguiar-Santos a , Amélia Maciel b , Zulma Medeiros a,e a

Parasitology Department, Aggeu Magalhães Research Center, Oswaldo Cruz Foundation, PE, Brazil Postgraduate Course on Tropical Medicine – Federal University of Pernambuco, PE, Brazil c Social Research Department, Joaquin Nabuco Foundation, PE, Brazil d Secretary of Health of Jaboatão dos Guararapes, PE, Brazil e Pathology Department, Institute of Biological Sciences, University of Pernambuco, PE, Brazil b

a r t i c l e

i n f o

Article history: Received 16 February 2011 Received in revised form 9 May 2011 Accepted 17 June 2011 Available online 24 June 2011 Keywords: Lymphatic filariasis Children Morbidity surveys Disease map Spatial analysis Control programs

a b s t r a c t A parasitological survey was conducted among children and adolescents in the municipality of Jaboatão dos Guararapes, Brazil to describe the occurrence and spatial distribution of lymphatic filariasis. Microfilaraemia was investigated through the thick smear technique, using 50 ␮l of capillary blood that was collected at night. The spatial analysis used a digital base map of the municipality, divided into districts, which were classified as hypoendemic, mesoendemic or hyperendemic. 8670 children were examined and 96 cases of microfilaraemia were identified (1.1%). The prevalence rate did not differ significantly between the sexes. Occurrences of filarial infection increased with increasing age: the greatest prevalence was recorded between 15 and 18 years of age (P < 0.05). There were 49 reports of clinical manifestations. The spatial distribution of microfilaraemia according to residential district showed that 13 (54.2%) of the 24 districts investigated were positive. Approximately 33% of the districts were hyperendemic. The results demonstrated that the pediatric population had intense early exposure to the parasite, thus characterizing filariasis as endemic in the municipality. The spatial analysis allowed identification of areas with greater occurrence of infection among children, and showed localities where the populations most exposed to transmission were concentrated. Epidemiological surveillance of microfilaraemia among children and spatial analysis are important local transmission indicators and form instruments for planning actions within the Global Program to Eliminate Lymphatic Filariasis, since they make it possible to identify priority areas. © 2011 Elsevier B.V. All rights reserved.

Lymphatic filariasis affects around 22 million children and adolescents aged under 15 years, living in 81 countries around the world (Michael et al., 1996; WHO, 2008). The prevalence of filariasis is directly related to local transmission, and the infection rate among children is a sensitive indicator of endemicity (Witt and Ottesen, 2001). In Brazil, which is a cosignatory of the Global Program to Eliminate Lymphatic Filariasis (GPELF), the actions are focused on the metropolitan region of Recife (Olinda, Jaboatão dos Guararapes, Recife and Paulista), the only endemic region for Wuchereria bancrofti in this country (Maciel et al., 1996; Medeiros et al., 1999, WHO/CDS/NTD, 2006). Epidemiological surveys (Braga et al., 1997, 1998, 2005), clinical studies (Dreyer et al., 1999, 2001) and ther-

∗ Corresponding author at: Centro de Pesquisas Aggeu Magalhães CPqAM/Fiocruz Av. Professor Moraes Rego, s/n, 50670-420, Cidade Universitária, Recife, PE, Brazil. E-mail addresses: brandaoe@cpqam.fiocruz.br, [email protected] (E. Brandão). 0001-706X/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.actatropica.2011.06.004

apeutic studies (Rizzo et al., 2007) carried out in this endemic area have indicated that information is needed on the spatial distribution and risk status of filarial infection among the pediatric population. In view of these gaps, the present study was conducted with the aim of describing the prevalence of filarial infection and morbidity among children and adolescents and the spatial distribution of this infection, in the municipality of Jaboatão dos Guararapes, pre mass drug administration (MDA). The minimum sample size (6920 individuals) was estimated based on the total number of population aged 0–18 years recorded in the last census (231,383), assuming that 1.7% of microfilaraemia, a design effect of 0.30 and a standard error of 1.0, with a 95% confidence interval. Households were selected in the 24 districts by going through the 484 census tracts (CT). Fourteen households per CT were selected based on the maps used in the last national census. The map of each CT was divided into four quadrants and then a straight line bisecting the second and third quadrants was drawn. A middle point is located in these two quadrants and two streets are selected. Seven households are researched in each street, which

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Table 1 Prevalence of microfilaremia according to sex, age group and clinical complaints, in the municipality of Jaboatão dos Guararapes, Pernambuco, Brazil. Variables

Microfilaremic

%

Amicrofilaremic

%

Total N

Sex Male Female Total Age group in yearsa 1–5 6–9 10–14 15–18 Total Clinicalb Erysipela/Elephantiasis Lymphoedema Hydrocele Milky Urine Asymptomatic Total District Cavaleiro Jaboatão Prazeres Total a b

Statistic %

OR

2

P

0.01 – –

0.91 – –

48 48 96

1.1 1.1 1.1

4.193 4.381 8.574

98.9 98.9 98.9

4.241 4.429 8.670

48.9 51.1 100.0

1.04 1.00 –

0 11 42 43 96

0.0 0.6 1.5 1.9 1.1

1.882 1.767 2.725 2.200 8.574

100.0 99.4 98.5 98.1 98.9

1.882 1.778 2.767 2.243 8.670

21.7 20.5 31.9 25.9 100.0

Reference group 1.00 – 2.48 6.83 3.14 11.66 – –

0 0 1 0 95 96

0.0 0.0 12.5 0.0 1.1 1.1

38 0 7 3 8.526 8.574

100.0 0.0 87.5 100.0 98.9 98.9

38 0 8 3 8.621 8.670

0.4 0.0 0.1 0.0 99.5 100.0

– – 12.82 – 1.00

– – 1.92 –

– – 0.08 –

59 11 26 96

1.7 0.7 0.7 1.1

3.455 1.527 3.592 8.574

98.3 99.3 99.3 98.9

3.514 1.538 3.618 8.670

40.6 17.7 41.7 100.0

2.36 1.00 1.00

13.16 0.03 –

0.00 0.89 –

– 0.00 0.00 –

Their mean age of population was 10.32 years and the mean age of these cases was 13.57 years. 18 age (post pubertal).

sum 14 households per CT. A total of 10,520 people were registered to participate in the survey, but 1850 of them (17.6%) did not undergo the test and thus a final sample of 8670 individuals was obtained. The presence of microfilariae was investigated by means of the thick smear technique, using samples of about 50 ␮l of capillary blood that were collected at times between 23:00 h and 01:00 h (Dreyer et al., 1996). These samples were used to prepare thick smears, which were Giemsa-stained and then checked under an optical microscope, for microfilariae of W. bancrofti. The analysis was descriptive and the data collected were stored and analyzed using EpiInfo version 6.04d. Statistical comparisons were made using the chi-square test (2 ), whenever appropriate. A P-value of <0.05 was considered indicative of a statistically significant difference. This study was approved by the Research Ethics Committee of the Aggeu Magalhães Research Center, Fiocruz (CAAE No. 0034.0.095.000-07). All the individuals who were positive for microfilariae were treated with diethylcarbamazine (WHO/CTD/TDR, 1994). To spatially analyze the information, the digital base map of the municipality of Jaboatão dos Guararapes was used. The data map was compiled using the TerraView software, version 3.5.0 (http://www.dpi.inpe.br/terraview/index.php). The technique of spatial analysis of data according to area was used. The districts were classified according to the prevalence of microfilaraemia, with stratification into terciles in which each band contained the same number of occurrences. The occurrences were classified as hypoendemic, mesoendemic and hyperendemic (Bonfim et al., 2009). In total, 8670 children and adolescents of both sexes were examined with a microfilaraemia prevalence of 1.1% (Table 1). The results from the survey highlighted the district of Cavaleiro, since this district presented a microfilaraemia prevalence rate that was greater (1.7%) than the general rate for the municipality. An epidemiological survey conducted among the general population had already indicated that the district of Cavaleiro was a locality with a wellestablished endemic process, given that it found a prevalence rate of 2.2%, with a range from 0 to 5.2% and presence of individuals with microfilaraemia in all the age ranges investigated (Bonfim et al., 2003).

In the age group of the present epidemiological survey, there was no association between sex and the presence of microfilaraemia (Table 1). This was contrary to the finding among the general population, in which greater prevalence was observed among males (Maciel et al., 1994; Bonfim et al., 2003; Rochars et al., 2004). These findings corroborate other surveys that investigated occurrences of lymphatic filariasis among children and adolescents and also did not find any significant difference between the sexes (Braga et al., 1997; Witt and Ottesen, 2001; Bal et al., 2009). The smaller proportion of cases of microfilaraemia and filarial disease among the female population after the age of 15 years may be attributed to differences in behavior that make males more exposed to bites from the vector insects, or to greater immunological resistance among females because of the influence of hormonal changes that occur during the reproductive period (Bradin, 1990; Albuquerque et al., 1995; Braga et al., 2005). Distribution of the children with microfilaraemia according to age group made it possible to show that the most recent cases of infection had occurred among children aged six years. Table 1 showed that the prevalence of the infection increased with increasing age, given that the highest rates were observed in the age range between 15 and 18 years (P < 0.05). These data corroborate other studies carried out in Haiti (Fox et al., 2005), Tanzania (Witt and Ottesen, 2001), India (Bal et al., 2009) and Brazil (Braga et al., 2005). According to Braga et al. (1997), this profile may be associated with changes in behavioral patterns that occur with increasing age, which make children who are close to adult age more exposed to infection, along with the physiopathogenic characteristics of lymphatic filariasis. With regard to clinical complaints, the results from this survey indicated that erysipelas and hydrocele were the complaints most mentioned among the individuals investigated, although only one individual presented microfilaraemia (Table 1). In areas that are endemic for lymphatic filariasis, the clinical manifestations of the disease are varied and appear more frequently in adulthood. Consequently, less attention has been paid to signs and symptoms during childhood (Figueiredo-Silva and Dreyer, 2005). According to data from the World Health Organization, out of the 120 million people infected worldwide, approximately 44 million have visible signs

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Fig. 1. Distribution of microfilaremia prevalence rates in the municipality of Jaboatão dos Guararapes, Pernambuco, Brazil.

of the disease (hydrocele or lymphedema), and another 76 million have preclinical manifestations (WHO/CTD/FIL, 1997). The presence of lymphedema in the limbs of children living in areas that are endemic for lymphatic filariasis has been reported (Ramaiah et al., 1996, 2000). However, such occurrences are rarer among children under the age of 10 years (Witt and Ottesen, 2001). In Brazil, a study on 11 children aged 9–15 years who were seen as outpatients and identified as carrying adult worms of W. bancrofti (detected by means of ultrasonography) found that one child had hydrocele and another had lymphadenopathy (Dreyer et al., 1999). Another study on 22 children aged 2–15 years who had adult worms found that the sites occupied by the worms were specific and distinct from what was observed among adult patients (Figueiredo-Silva and Dreyer, 2005). In the light of these findings, the importance of ultrasonography for evaluating this age group and identifying preclinical manifestations such as lymphangiectasia can be highlighted. It has been recognized that early detection and treatment of the parasitosis are fundamental for preventing chronic forms of this parasitosis (Shenoy et al., 2009). The spatial analysis on the distribution of occurrences of microfilaraemia according to residential district showed that positive cases occurred in 13 (54.2%) of the 24 districts investigated, with microfilaraemia prevalence rates ranging from 0 to 4.58% classified as hypoendemic, mesoendemic and hyperendemic (Fig. 1). It can be seen the areas with higher prevalence rates considered to be hyperendemic. These areas were on the border with areas of the city of Recife, a locality that is recognized to be endemic for filariasis (Medeiros et al., 2009). The spatial analysis made it possible to identify and characterize the areas with greatest occurrences of infection among children, and thus showing the localities in which the populations most exposed to filarial transmission were concentrated. An explanatory model for the endemicity of lymphatic filariasis in this region would need to presume that the infectious cycle is correlated with the population’s living conditions, especially with regard to people living in dirty areas with precarious environmental sanitation (Bonfim et al., in press). This type of analysis is an important tool for planning actions within the GPELF, since they make it possible to identify priority areas for control actions.

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