Introduction
Human schistosomiasis is a major health issue in many parts of Africa, Asia and Latin America. It is estimated that 200 million people, in 76 countries, are infected with one of the schistosome species that cause the disease (WHO, 2002). Although nearly 10–12 million people in Brazil were schistosome positive in the 1970s (Anon., 1977), control programmes have successfully reduced the related mortality, morbidity and transmission in Brazil. Similar results have been attained in China, Egypt and the Philippines (Andrade, Reference Andrade2002).
However, there are still around 2.5 million (Passos & Amaral, Reference Passos and Amaral1998) to 6.3 million (Katz & Peixoto, Reference Katz and Peixoto2000) individuals harbouring schistosomes in Brazil. In the state of Rio de Janeiro, some areas present low endemicity or isolated foci of schistosomiasis mansoni. In these areas, the prevalence of the disease is < 4% and most infected individuals have mild infections, excreting < 100 eggs/g faeces (Anon., 1994). In 1990, after several control programmes, the number of cases of schistosomiasis mansoni in the county of Paracambi reached a very low level, with only occasional transmission in some villages (Anon., 1994). Nonetheless, preliminary observations in the peri-urban village of Sabugo, which was undergoing an urbanization process, revealed contact points among streams, residential sewage and foci of Biomphalaria tenagophila (Orbigny, 1835) snails, including one in a residential water tank. This incomplete urbanization process was creating favourable conditions for the transmission of schistosomiasis in some areas of the village. Soares et al. (Reference Soares, Barreto, da Silva, Pereira, Moza, Rey, Calçado, Lustoza and Maspero1995) concluded that such a scenario could increase the intensity of infections, and that the low prevalence could mask a highly focal transmission in the village of Sabugo.
The aim of the present study was to assess the prevalence and intensity of Schistosoma mansoni infection and the transmission of schistosomiasis in Sabugo, as well as to follow up on the negative prognosis made around 15 years ago.
Subjects and methods
Study area, population and consent
This field study was carried out in 2005 in the village of Sabugo, located in a valley of Paracambi (2°35″S, 43°40″W), a county in the state of Rio de Janeiro, south-eastern Brazil. The Sabuguinho and Ingá streams, which are permanent and part of the basin of the Paraíba do Sul River, flow from the neighbouring rural villages of São José and Saudoso, respectively. They run 3 km through Sabugo. The climate is hot and humid, with a rainy season from December to February. Since the 1970s, the locality has undergone urbanization over a site originally known as ‘Fazenda Sabugo’ (Sabugo Farm), which in the past grew coffee and oranges.
At the beginning of this survey, the population was of approximately 1600 inhabitants living in 320 unevenly spread dwellings, comprising a mixed rural/urban environment. At a village-wide meeting prior to any investigations, the goals and methods of the study and the problems posed by human schistosomiasis were explained to the inhabitants of Sabugo. Informed consent was obtained from the adult subjects and the parents of the children investigated. The name, age, gender and address of each subject were recorded.
The study protocol was approved by the Ethics Committee of the Oswaldo Cruz Foundation, in the city of Rio de Janeiro (Certificado de Apresentação para Apreciação Ética 0038.0.011.000-03).
Stool examination
Faeces were evaluated by the free sedimentation (Lutz, Reference Lutz1919) and Kato-Katz (Katz et al., Reference Katz, Chaves and Pellegrino1972) methods, based on one stool sample per person and on two slides per sample per method, repeating the procedure adopted in 1990 and commonly used in the county until 2005. Intensity of infection was evaluated by the Kato-Katz method and classified as light, moderate or heavy if there were 1–99, 100–399 or over 400 eggs/g faeces, respectively (WHO, 2002).
Patient survey
Each individual found stool positive for S. mansoni eggs was asked about possible ways of infection, given a general clinical examination and treated with a single oral dose of 40 mg/kg praziquantel (WHO, 2002). The tablets were administered with milk to minimize any gastrointestinal side effects. During the standardized clinical examinations, the subjects were asked about the symptoms they had displayed in the previous 6 months. Cases in which the liver extended beyond the right costal margin in the sternal or mid-clavicular lines were defined as clinical hepatomegaly. Similarly, the spleen extending beyond the left costal margin was recorded as splenomegaly.
Snails
In order to identify snail-breeding sites, water reservoirs were surveyed. The percentage of S. mansoni infection at each snail-breeding site was determined by repeated exposure of collected snails to artificial light, every 5 days for 45 days (Standen, Reference Standen1952).
Results
Infection levels
Overall, 1356 individuals provided faecal samples. Age was known for 1311 (96.7%) individuals, ranging from 0 to 90 years with a median of 30.7 years. The majority (63.9%) of the participants were over 19 years old. Thirteen (1%) individuals had schistosomiasis. Although there were more female than male subjects (712 vs. 644) in the study, there was a predominance of males with S. mansoni (10 vs. 3). Infected people were aged 8–55 (median: 33.7 years). One 8-year-old patient was the only one under 15 years old.
All patients had the intestinal or hepato-intestinal forms of the disease. The parasitological load was light in eight (61.5%) of the infected patients, moderate in four (30.8%) and heavy (528 eggs/g faeces) in only one patient (7.7%). Eleven patients were infected in Sabugo and one in another village of Paracambi; it was not possible to determine the site of infection of one patient. Leisure activities (fishing and bathing) in the Sabuguinho stream were the main origins of infection.
Snail survey
The search for B. tenagophila was positive in five sites around the Sabuguinho and Ingá streams and nearby marshes. Infected snails were only found in one station of the Sabuguinho stream, close to a waterfall used by people for leisure activities. Out of 19 snails, 3 (15.8%) were infected, representing a high infection rate.
Discussion
Soares et al. (Reference Soares, Barreto, da Silva, Pereira, Moza, Rey, Calçado, Lustoza and Maspero1995) showed that an incomplete urbanization process due to poverty, lack of information and, above all, the conditions of a destitute urban community may favour the transmission of S. mansoni, possibly causing more harm than in rural environments.
Schistosomiasis is strongly related to poor socioeconomic conditions (Kloetzel, Reference Kloetzel1989; Loureiro, Reference Loureiro1989). The growing number of cases in urban areas (Mott et al., Reference Mott, Desjeux, Moncayo, Ranque and De Raadt1990) is associated with the settlement of peripheral areas without the appropriate provision of services and basic infrastructure. The county of Paracambi, an isolated focus of schistosomiasis, is not an exception: most of its urban area is inhabited by low-income individuals, and the occupation of peripheral areas is related to unemployment and housing problems, among others, which create or aggravate sanitation issues. The streams have become the obvious solution for waste disposal. Moreover, the absence of treated water in two of the poorest and most densely populated peri-urban areas of the locality has induced the domestic use of water from natural and untreated sources.
Consequences of this urbanization process in Sabugo have been striking. First streams reach the peri-urban zone polluted by stools from the rural areas, and the higher concentration of houses increases their contamination. Second since the Sabuguinho stream runs through the backyards of many houses and holds small fish and crustacea, human contact with the water is almost unavoidable, despite its unpleasant smell and appearance. Third in contrast to the rural areas, where there are several springs and few houses, the peri-urban areas have relatively large populations competing for a small number of distant springs. Therefore, people have no other choice than to use water from the Sabuguinho stream, thus spreading the snail colonies and setting up potential transmission sites among the dwellings. As shown in our previous study (Soares et al., Reference Soares, Barreto, da Silva, Pereira, Moza, Rey, Calçado, Lustoza and Maspero1995), those in contact with snail-infected water presented a statistically higher risk of infection.
Nonetheless, comparing our results with the prognostic made in the study carried out in 1990 (Soares et al., Reference Soares, Barreto, da Silva, Pereira, Moza, Rey, Calçado, Lustoza and Maspero1995), we can conclude that it was not confirmed. The number of patients decreased, as did the intensity of infections. In 1990, out of 1103 individuals, there were 27 (2.7%) cases of schistosomiasis against 13 (1%) in 2005. While the proportion of light infections increased, moderate or heavy infections decreased from 51.85% in 1990 to 38.5% in 2005. Heavy infections dropped from 43.75 to 7.7%. However, it is worth noting that the prevalence of light infections is as expected in low prevalence areas (WHO, 1985; Katz, Reference Katz, Reis, Faria and Katz1986; Dias et al., Reference Dias, Marçal, Glasser, Kanamura and Hotta1992).
In spite of this disagreement between present results and previous negative prognostics, schistosomiasis in Sabugo still deserves special attention, since 15 years later transmission still occurs. Moreover, the diagnostic techniques used on both occasions bear a considerable risk of underestimating the number of detected cases. Reasons for the disagreement between the rather pessimistic prognostic in the 1990s and the present results are difficult to identify but one hypothesis is that the evident increase in the pollution of water sources in Sabugo led to a reduction in contact with this water.
This work evidences the need for a better understanding of schistosomiasis in low-endemic situations. First, and foremost, the low worm burden of most cases in the locality under study indicates the need for more efficient diagnostic methods in order to avoid underestimation of prevalence. Hoshino-Shimizu et al. (Reference Hoshino-Shimizu, Dias, Kanamura, Silva, Glasser and Patucci1992) and Noya et al. (Reference Noya, Ruiz, Losada, Colmenares, Contreras, Cesari and Noya2007) recommend serological methods, while Barreto et al. (Reference Barreto, Smith and Sleigh1990) and Rabello et al. (Reference Rabello, Rocha, Mendes de Oliveira, Katz and Lambertucci1992) have shown that the efficiency of the Kato-Katz method can be improved if a larger number of samples is analysed. Gonçalves et al. (Reference Gonçalves, Barreto, Peralta, Gargione, Gonçalves, Igreja, Soares and Peralta2006), working in a low prevalence area, observed a 41% increase in the cases by examining three stool samples instead of one, and a seroprevalence five times higher than parasitological prevalence. Enk et al. (Reference Enk, Lima, Drummond, Schall and Coelho2008), also working in a low transmission area, observed an increase in schistosomiasis prevalence from 3.8% with one Kato-Katz slide to 27.2% with ten Kato-Katz slides of three stool samples, and to 35.4% using the formol ether centrifugation technique, indicating that prevalence in that area was underestimated. Since only one stool sample was examined in the present study, it is likely that a larger number of infected patients could have been identified had more stool samples been analysed.
Schistosomiasis in Brazil occurs mainly as a low prevalence disease even in hyperendemic areas in the north-east (Rey, Reference Rey1990), and epidemiologic studies in low prevalence areas and isolated foci of schistosomiasis have been carried out. Dias et al. (Reference Dias, Glasser, Etzel, Kawazoe, Hoshino-Shimizu, Kanamura, Cordeiro, Marçal, Carvalho, Gonçalves and Patucci1988, Reference Dias, Marçal, Glasser, Kanamura and Hotta1992) and Marçal et al. (Reference Marçal, Patucci, Dias, Hotta and Etzel1991) found that controls had not been completely developed yet and that the prevalence indices were still alarming. Coura-Filho et al. (Reference Coura-Filho, Rocha, Lima e Costa and Katz1992) reported that 10 years after having started control measures in Peri-Peri, a county in the state of Minas Gerais in Brazil, the prevalence of schistosomiasis dropped from 43.5 to 15.2%, and as low as 4.4% 3 years later. However, 3 years after the end of the control programme, the prevalence increased to 19.6%. Such a study shows that low-prevalence schistosomiasis should never be neglected. In Sabugo, despite the low endemicity, transmission has not ceased, and cases of moderate and heavy infections are still being reported.
Another reason to invest in studying low-endemic situations is related to some important differences, which set them apart from medium and high endemic scenarios. As in 1990, young males were the most affected group. Working in a nearby village, Igreja et al. (Reference Igreja, Mattos, Gonçalves, Barreto and Peralta2007) also observed the highest prevalence of S. mansoni infection among young males. Young children are usually a high-risk group for schistosome infection (Jordan & Webbe, Reference Jordan, Webbe, Jordan, Webbe and Sturrock1993; Raso et al., Reference Raso, N'Goran, Toty, Luginbühl, Adjoua, Tian-Bi, Bogoch, Vounatsou, Tanner and Utzinger2004). Bina & Prata (Reference Bina and Prata2003), working in a highly endemic area of Brazil, examined 367 children aged 0–9 years old and found that 33.2% of them were excreting eggs. Burlandy-Soares et al. (Reference Burlandy-Soares, de Souza Dias, Kanamura, de Oliveira and Ciaravolo2003), on the other hand, working in a low-endemic area of the same country, observed a shift in the age group with highest prevalence of infection, from adolescents (aged 15–19) in 1980 to older adults (aged 25–29) in 1998. This change was attributed to a relatively low prevalence in the subjects aged 15–19 in 1998, as they had been born after the intensification of a schistosome control programme in the study area.
Therefore, we should target young men performing leisure activities, our at-risk population, in future prophylactic measures, such as warning about the danger of fishing and bathing in the Sabuguinho stream. Schoolchildren from 7 to 14 years of age were not found to have schistosomiasis in Sabugo, unlike the situation in highly endemic areas.
For the short- and long-term control of schistosomiasis in Sabugo, changes in the socio-ecologic, socio-cultural and bio-ecologic levels of transmission are needed, besides chemotherapy synchronized with snail control. Such measures require investments especially in sanitation, which is also desirable for other reasons. This cannot be considered a utopian goal (Kloetzel, Reference Kloetzel1989), and is recommended by the World Health Organization (1993). Individual initiatives seem to be hindered mainly by the following factors related to the low socio-economic level of this community: (1) the cost of conducting water of good quality is high, since both treated water and the few sources of good-quality untreated water are very far away; (2) fishing and bathing in the streams, as well as soccer playing (which leads to frequent contact with the transmission sites), are free leisure activities, easily available in the locality; (3) building and maintaining septic tanks are costly and involve techniques that the community at large does not know.
Soares et al. (Reference Soares, Barreto, da Silva, Pereira, Moza, Rey, Calçado, Lustoza and Maspero1995) concluded that low prevalence and low intensity of infections could mask a highly focal transmission. Accordingly, our study has revealed the existence of high-risk groups and foci with substantial transmission potential, similar to foci in more highly endemic areas. Therefore, it is clear that, in order to set up a control programme suitable to this locality, epidemiological research is required with the purpose of identifying peculiarities related to the intensity, morbidity and transmission of infections, as well as locating the transmission foci and clusters of infected people, and the risk factors to be targeted by control efforts.
Acknowledgements
This work was supported by Fundação Oswaldo Cruz, PDTSP – Águas and Prefeitura Municipal de Paracambi. We would like to thank Edvaldo Xavier for technical assistance and Jacqueline O. Alonso for institutional support at the Zoonosis Control Center.
