Memórias do Instituto Oswaldo Cruz Fundação Oswaldo Cruz, Fiocruz ISSN: 1678-8060 EISSN: 1678-8060 Vol. 104, Num. 8, 2009, pp. 1159-1164

Memórias do Instituto Oswaldo Cruz, Vol. 104, No. 8, 2009, pp. 1159-1164

ARTICLES

Surveillance of Chagas disease vectors in municipalities of the state of Ceará, Brazil

Teresa Cristina Monte Gonçalves^{I, +}; Assilon Lindoval Carneiro Freitas^II; Simone Patrícia Carneiro Freitas^I

^ISetor de Entomologia Médica e Forense, Laboratório de Transmissores de Leishmanioses, Instituto Oswaldo Cruz-Fiocruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil
^II20ª Célula Regional da Saúde, Crato, CE, Brasil
+ Corresponding author: tcmonte@ioc.fiocruz.br

Received 15 June 2009
Accepted 19 October 2009

Code Number: oc09231

ABSTRACT

The present study aimed to analyse the dwelling infestation rates and the distribution and natural Trypanosoma cruzi infection rates, among triatomines captured in the 13 municipalities of the state of Ceará. The records relating to the capture of intradomicile and peridomicile triatomines during the Chagas disease control program of 1998-2008 were available. Among the triatomines captured and in all of the municipalities studied, Triatoma brasiliensis presented the highest incidence in intradomicile and Triatoma pseudomaculata in peridomicile and some were positive for infection by T. cruzi. We emphasise that it is important to have sustainable epidemiological surveillance in the region, since when the control measures decreased, the incidence of T. pseudomaculata in intradomicile grew.

Key words: Triatominae - distributions - natural infection - Ceará

Northeastern Brazil is a macroregion in which Chagas disease occurs endemically. A variety of vector species for the parasite Trypanosoma cruzi that are of public health importance are found in this region: Triatoma brasiliensis Neiva 1911, Triatoma pseudomaculata Corrêa & Espínola 1964, Panstrongylus lutzi (Neiva & Pinto 1923) and Panstrongylus megistus Burmeister 1835 (Dias et al. 2000, MS 2005).

The species T. brasiliensis, T. pseudomaculata and P. lutzi are native to the area and have a wide distribution across the semi-arid zones of the Northeastern region. In control program surveys, the first two species were considered to be potential vectors because they form colonies in homes, leading to a continual risk of vector transmission (MS 2005). Regarding their feeding habits, T. brasiliensis is moderately anthropophilic and T. pseudomaculata is ornithophilic (Forattini et al. 1981, Silveira et al. 1984, Freitas et al. 2005).

In 1975, the vector control actions for Chagas disease in Brazil became systematised and the programs attained nationwide scope (Silveira et al. 1984). In 2000, the epidemiological surveillance was maintained in the areas covered by decentralisation of health services, when municipalities then started to carry out the actions within the program (Diário Oficial da União 2004).

The present paper analyses the dwelling infestation rates and the distribution and natural T. cruzi infection rates among triatomine species that occur in the municipalities that make up the 20ª Célula Regional da Saúde (CERES) of the state of Ceará (CE). These results will provide information regarding the present situation of the Chagas disease control programs in these municipalities.

MATERIALS AND METHODS

CE covers an area of 148,016 km² and has a coastline extending for 538 km. Most of this area consists of topographically low-lying, semi-arid terrain (Alencar et al. 1976).

In the present paper, records relating to triatomine capture during the Chagas disease control program of 1998-2008 were analysed. These records were from 13 municipalities: Altaneira, Antonina do Norte, Araripe, Assaré, Campos Sales, Crato, Farias Brito, Nova Olinda, Potengi, Salitre, Santana do Cariri, Tarrafas and Várzea Alegre. This region covers an area of 8.686 km² and is located in the Cariri region of the southern CE, at the boundaries of the states of Piauí and Pernambuco (between latitudes 6º41'40"N and 7º39'00"S and longitudes 39º37'20"E and 40º30'00"W). The Cariri region has a hot climate for most of the year and its vegetation is predominantly caatinga.

Specimens were captured intradomicile and peridomicile, in rural localities, according to Manual de Normas Técnicas da Superintendência de Campanhas de Saúde Pública (MS 1980). In addition, the prevalence of the distribution of the vector species and the occurrence of natural infection by T. cruzi in triatomines were ana-lysed as indicators for the relationship between triatomines and T. cruzi and as operational indicators.

According to standard Pan American Health Organization procedures (PAHO 2007), the following rates were calculated: the infestation rates of each of the municipalities (number of positive homes x 100/total number of examined homes), the infestation peridomicile rates (number of homes with vectors in peridomicile x 100/number of examined homes with peridomicile), the infestation intradomicile rates (number of homes with vectors in intradomicile x 100/number of examined homes with intradomicile), the dispersion rates (number of locality infested x 100/total number of locality examined) and the natural infection rates by T. cruzi, represented by the number of infected vectors x 100/number of examined vectors.

RESULTS

In the 13 municipalities studied, between 1998-2008, a total of 36,204 triatomine specimens were captured, 10,740 adults and 25,464 nymphs. Among these, the highest number species captured was T. pseudomaculata, with a prevalence of nymphs in peridomicile. This was followed by T. brasiliensis, which also presented with a higher number of nymphs in peridomicile.

Rhodnius nasutus Stål, 1859, followed, also with the highest number of nymphs in peridomicile and with a low prevalence in intradomicile. In addition, other captured species were P. lutzi which had the greatest number of insects captured as adults in intradomicile and P. megistus, which similarly had the highest number of nymphs in peridomicile (Table I).

In 2001, the greatest number of specimens was captured, with a total of 6,623 (18.29%) specimens. This was followed by 2005 with 5,542 (15.3%), 2004 with 3,480 (9.61%), 2002 with 3,358 (9.27%), 2006 with 3,241 (8.95%), 1999 with 2,987 (8.25%), 2007 with 2,881 (7.96%), 1998 with 2,834 (7.82%), 2003 with 2,737 (7.6%); 2008 with 1,748 (4.82%), and 2000 with 773 (2.13%) (Fig. 1).

The T. brasiliensis species had the high prevalence in intradomicile in all of the years and municipalities, followed by T. pseudomaculata, P. lutzi, R. nasutus and P. megistus (Fig. 2, Table IIa and b). The lower rates of triatomines in the intradomicile and peridomicile were observed in the municipalities of Altaneira, Crato and Nova Olinda. On the other hand, higher rates occurred in Potengi, Assaré and Várzea Alegre (Table III). The city of Várzea Alegre had not only the highest number of homes with insects, but also had the highest dispersion rates (Table III).

Várzea Alegre had the highest number of triatomines infected with T. cruzi with 64 insects infected; 10 of the insects were T. brasiliensis (4 adults and 3 nymphs), 53 were T. pseudomaculata (23 adults and 30 nymphs) and one adult was P. megistus. The municipalities of the Altaneira and Antonina do Norte had the lowest number of infected insects, with only one adult and two nymphs of T. pseudomaculata and one adult and one nymph of T. brasiliensis. However, the highest natural infection rates were recorded in the city of Araripe, while the lowest rates were recorded in Antonina do Norte. With regard to species, T. pseudomaculata had the highest number of positive specimens, although P. megistus and P. lutzi had the highest natural infection rates (Supplementary data).

DISCUSSION

The operational procedures of the Fundação Nacional de Saúde have been detailed and their impact on endemic disease monitoring and vector control in nine states of Northeastern Brazil has been analysed. Previous studies have put an emphasis on the process of domestication of triatomines in different regions of Northeastern Brazil, thus providing a warning about future public health problems (Alencar et al. 1976, Dias et al. 2000, Costa et al. 2003, Sarquis et al. 2004, 2006).

All of the species were captured both intradomicile and peridomicile. The latter environment had a greater prevalence of vectors, which may indicate the possibility of acceleration in the process of intradomicile re-infestation. The process of intradomicile re-infestation is influenced by the existence of animals in peridomicile and the shelter conditions that the vector finds in the human habitation (Silveira et al. 2001, Freitas et al. 2004b).

The highest number of captured insects in all of the municipalities was T. pseudomaculata. However, currently, T. brasiliensis still exhibits the highest number of captured specimens in intradomicile in the Cariri region and has not yet been replaced by T. pseudomaculata. Although, it has been suggested that a process of replacement of T. brasiliensis by T. pseudomaculata may be occurring (Silveira et al. 2001). In addition to this region, T. pseudomaculata has also been found in wild environments (Freitas et al. 2004b).

The low number of vectors captured in the municipalities of Altaneira, Antonina do Norte, Nova Olinda and Salitre could be due to several factors. In Altaneira, the captures were constantly interrupted and were sometimes not performed; this is apparent in data from the research activity of 20ª CERES, where the municipality activities started on 2001. Moreover, the territorial extension of the municipality is the smallest of the other 12 covered by CERES, which also could lead to a number lower. In Antonina do Norte and Salitre (personal communication), the infestation might be higher; however, the lack of systematisation of services has compromised the number of notifications. It is important to emphasise that Antonina do Norte borders the municipalities of Campos Sales, Tarrafas and Assaré, and Assaré is the municipality that has both high rates of infestation and dispersion.

It is important to draw attention to the surveillance services in Assaré, Potengi and Várzea Alegre, since infestation rates and dispersion of triatomines in these municipalities show the highest rates. This may be due to the presence of factors such as environmental conditions, vegetation, food, territorial proximity and the use of wood for building animal shelters (Freitas et al. 2004b); all of which can influence the dispersion of triatomines to areas that are typically not covered in the surveillance, contributing to the maintenance of triatomines in region.

The low natural infection rates by T. cruzi in the Cariri region may be due to the fact that most species have been collected in peridomiciliary annexes, where the predominant food source is the blood of birds (Freitas et al. 2005). Moreover, the CERES, responsible for laboratory analysis of insects sent by several municipalities, continually have difficulty in analysing the volume of material, leaving the vectors in a period of fasting. This starvation sometimes causes death and according to the protocol used by the CERES, these insects are then not analysed. It is important to emphasise that although low, the rates of infection in T. brasiliensis and T. pseudomaculata are important, since these insects are found primarily in intradomicile and peridomicile, at all stages of development, and have a food source that is the blood of domestic animals and humans, which keeps the Chagas disease cycle present in these environments.

The same attention needs to be given to R. nasutus, which is a species predominantly found in wild habitats. R. nasutus has often been found to colonise artificial ecotopes in peridomicile and are sometimes infected with T. cruzi (Silveira & Vinhaes 1998, Sarquis et al. 2004) or have a mixed infection with Trypanosoma rangeli (Dias et al. 2008). The authors of the last paper suggest the need for epidemiological surveillance in the region of the Chapada do Araripe, since that palm trees close to home are infested with R. nasutus that are infected by T. cruzi, demonstrating the importance of maintenance of sylvatic T. cruzi transmission in this area.

According to PAHO (2007), the rate of colonisation is related to the number of domiciles, with nymphs x 100/number of homes inspected. In this study, the rate of colonisation established by PAHO (2007) could not be evaluated because the work performed by the CERES did not consider the exact number of nymphs per domicile examined. Thus, it is suggested the colonisation of wild species has occurred, since R. nasutus, due to the presence of nymphs in the homes, has been found annually in the region.

It is now considered that there is a risk of Chagas disease transmission due to the presence of emerging species such as P. lutzi (Freitas et al. 2004a). Therefore, there is a risk that the invasion by this vector may continue or persist, since the characteristics of the peridomicile (such as presence of the vector in wild environments and the presence of food) may influence the process of invasion and colonisation of the home (Freitas et al. 2004a, MS 2005). In this region, adults of this species were found to have greater capture rates in intradomicile, facilitating colonisation in this environment. Since environmental conditions were not considered in the CERES data, we suggest that P. lutzi and R. nasutus have remained in intradomicile because of the rainy season, which undermines the work of spraying.

Over the 11 years of the Chagas disease Control Program in 20ª CERES, there was a considerable increase in the results in 2001 and 2005. This was caused by an increase in the number of endemic disease control agents, who formed specific teams for Chagas disease and dengue control (personal communication). However, the sudden decrease that follows after these two years (2001 and 2005) represent a break from work and consequently, a decrease in the number of insects that were captured.

These results empathise previous studies in different areas (Costa et al. 2003, Sarquis et al. 2006, Freitas et al. 2007), showing the importance of the epidemiological surveillance in the Cariri region of CE. The work indicates that surveillance must be sustainable, considering that T. pseudomaculata and T. brasiliensis are native, present in the human environment of all of the municipalities and infected by T. cruzi.

Supplementary data

ACKNOWLEDGEMENTS

To the Health Departments of the 13 municipalities that make up 20ª Célula Regional da Saúde, CE, for their support and the data supplied, and to the endemic disease agents, for capturing triatomines in the field.

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