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Impact of control measures and dynamics of sand flies in southern Brazil

2013; Wiley; Volume: 38; Issue: 1 Linguagem: Inglês

10.1111/j.1948-7134.2013.12009.x

1948-7134

Kárin Rosi Reinhold-Castro, Vanderson Carvalho Fenelon, Robson Marcelo Rossi, João Eduardo Cavalcanti Brito, Janaína Sales de Freitas, Ueslei Teodoro,

Trypanosoma species research and implications

We report the results of control measures introduced to reduce the density of sand flies in domiciles and subsequent monitoring of the effects of these measures on the sand fly populations. The most common species of sand flies were Nyssomyia neivai and Nyssomyia whitmani, which are naturally infected by Leishmania. A total of 268,382 (93.4%) sand flies were collected in ecotypes constructed with the aim of attracting sand flies, and 19,091 (6.6%) sand flies were collected in the ecotypes consisting of residences and other buildings. Human actions determine the growth or reduction of the sand fly population in human-occupied space. Understanding the dynamics of sand flies in this environment can substantially contribute to the prevention of cutaneous leishmaniasis. Leishmaniasis occurs on four continents and currently affects 88 countries. Most cases (90%) of cutaneous leishmaniasis occur in Afghanistan, Brazil, Iran, Peru, Saudi Arabia, and Syria. However, the number of cases of cutaneous leishmaniasis has been underestimated because of lack of reporting in remote rural areas and because reporting is not compulsorily in 33 countries where it is endemic. In Latin America, the incidence of cutaneous leishmaniasis (CL) has been high, especially in Brazil, where the wide geographical distribution shows the importance of this disease. In southern Brazil, most cases of CL were recorded in the state of Paraná. In the Neotropical region, there are 480 species of sand flies and 229 of these occur in Brazil, although only some of them are involved in the transmission cycle of Leishmania (Aguiar and Medeiros 2003). In the state of Paraná, Ny. whitmani (Antunes and Coutinho), Ny. neivai (Pinto), Migonemyia migonei (France), Pintomyia pessoai (Coutinho and Barretto), and Pintomyia fischeri (Pinto) are always present in most localities where sand flies were collected and they might be important in the epidemiology of CL (Silva et al. 2008, Teodoro et al. 2010). Sand flies have been controlled by employing chemical insecticides on the walls of houses, silos, animal shelters, and other domestic buildings (Deane et al. 1955, Gratz 1999, Alexander and Maroli 2003) and impregnated in nets (Alexander and Maroli 2003, Picado et al. 2010). However, the sporadic use of insecticides during inappropriate periods and poorly constructed housing have limited the success of this tactic (Alexander and Maroli 2003, Alencar 1983). Moreover, because these insects are not closely associated with the domicile, the residual effect of insecticides is eliminated once they return to this environment (Marcondes 2011). The use of insecticides in natural environments represents a danger to non-target organisms and a high cost for achieving adequate coverage of forest areas, making the method impractical in these situations (Alexander and Maroli 2003, Marcondes 2011). Moreover, information on the location of breeding sites of sand flies is scanty (Marcondes 2011). Sand fly control measures that can be incorporated into the routine of people living in risk areas can reduce the density of these insects in the domicile and peridomicile, reducing the incidence of CL. Several studies have shown that the presence of hen houses in the peridomicile decreases the density of sand flies in the domicile and also their contact with humans when the hen houses are located at a distance of approximately 100 m from domiciles (Teodoro et al. 2001, Teodoro et al. 2003, Teodoro et al. 2007a). This is the fifth study in the Recanto Marista. The first described the fauna, the frequency of sand flies in the domicile, domestic animal shelters in the peridomicile, and the environmental conditions (Teodoro et al. 2001). The second study (Teodoro et al. 2003) described the measures introduced to reduce the density of sand flies in the domicile, and the subsequent reports (Teodoro et al. 2007b, Reinhold-Castro et al. 2008) described the monitoring of the results of these measures. In the present study, we evaluated the population dynamics of sand flies as affected by small daily changes in the human-altered environment and in the natural surroundings. Sand flies were caught in the Recanto Marista, municipality of Doutor Camargo (23° 33′ S and 52° 13′ W) in north-central Paraná. The area of Recanto Marista was described previously (Teodoro et al. 2003). Sand flies were collected with Falcão light traps, twice a month, from 22:00 to 02:00 each night, from July, 2006 to November, 2007, for a total of 136 hours per trap. The hourly collection schedule was the same as in previous studies in Recanto Marista (Teodoro et al. 2001, Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008). The traps were installed in the following ecotypes: Ecotype 1 (E1): on the porch of a residence at the entrance of the Recanto Marista; Ecotype 2 (E2): in a hen house next to another animal shelter built in January, 2006 where sheep and cattle take refuge at night; Ecotype 3 (E3): in the foundation of a house that is occasionally rented to visitors; ecotype E3 corresponds to the ecotype R of the previous study (Reinhold-Castro et al. 2008); Ecotype 4 (E4): an addition next to a house where temporary workers are occasionally housed; Ecotype 5 (E5): a hen house at a distance of 40 m from a house (E6); Ecotype 6 (E6) on the porch of a residence; Ecotype 7 (E7): a hen house 15 m distant from a house (E6); Ecotype 8 (E8): the main entrance of a lodge on the banks of the Ivaí River used by groups of people as a spiritual retreat; Ecotype 9 (E9): a hen house behind the lodge; Ecotype 10 (E10): a hen house on the right side of the lodge in the woods; Ecotype 11 (E11): a hen house built in June, 2002, near the gate of the Recanto Marista with the aim of attracting sand flies from ecotype E1. The measures employed to reduce the density of sand flies in peridomestic habitats were: i) removal of fallen leaves and fruit, agricultural residues, animal feces, the remains of food offered to them, and other types of soil organic matter, ii) providing appropriate disposal for water for domestic use and preventing it from soaking the soil around the houses. In addition to these measures, buildings (houses, barns, and others) and domestic-animal shelters were sprayed with an insecticide to control sand flies (Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008). The hen houses were constructed previously (Teodoro et al. 2003) to act as zooprophylactic barriers. The hen houses are lighted at night with 40 to 60W lamps in order to attract sand flies; on the sampling nights, they were not lighted. The sand flies were prepared and identified in the Laboratory of Parasitology, Department of Basic Health Sciences of the Universidade Estadual de Maringá (UEM). The nomenclature of the species follows Galati (2003), and the abbreviations of the sand fly genera follow Marcondes (2007). The temperature was measured at the beginning and end of each collection of sand flies. From July, 2006 to November, 2007, the mean temperature was 22.8° C at 22:00 and 19.9° C at 02:00. During this period, the total rainfall was 2,112.6 mm. The rainfall data were provided by the Weather Station of the UEM. The Mann-Whitney statistical test was used to compare the total numbers of Ny. whitmani and Ny. neivai collected. Nonparametric ANOVA Kruskal-Wallis and their respective multiple comparisons were used to compare the samples taken in different ecotypes. The same procedure was used to compare the period in which the number of sand flies collected increased, with the previous and subsequent periods, in ecotype 5 (E5). The Mann-Whitney test was used to compare the hourly means (HM) from the periods 2005/2006 and 2006/2007. For the tests, we used the software Statistica (StatSoft, Inc., 2010; STATISTICA data analysis software system, version 9.0), with a significance level of 5%. The results of this study are compared with the results of the study period in 2005/2006 (Reinhold-Castro et al. 2008). The sand flies collected were Brumptomyia brumpti (Larrousse), Brumptomyia cunhai (Mangabeira), Evandromyia cortelezzii (Brèthes), Expapillata firmatoi (Barretto, Martins & Pellegrino), Mi. migonei (France), Ny. neivai (Pinto), Ny. whitmani (Antunes & Coutinho), Pi. fischeri (Pinto), Pintomyia monticola (Costa Lima), Pi. pessoai (Barreto & Coutinho), and Psathyromyia shannoni (Dyar). Of the total 287,473 sand flies collected, Ny. neivai (87.4%) and Ny. whitmani (10.9%) predominated, representing 98.3% of the total (Table 1). The Mann-Whitney statistical test indicated a significant difference between the total numbers of Ny. whitmani and Ny. neivai collected (p=0.005237). Multiple comparisons indicated significant differences among the numbers of sand flies collected in the different ecotypes, as shown in Table 2. A total of 268,382 (93.4%) sand flies were collected in ecotypes E2, E5, E7, E9, E10, and E11, constructed with the aim of attracting sand flies (Table 2). In the other ecotypes (E1, E3, E4, E6, E8), represented by houses and other buildings, 19,091 (6.6%) sand flies were collected (Table 2). The Mann-Whitney test showed a significant difference between the number of sand flies collected in hen houses and in the other ecotypes (Table 2). The number of sand flies collected in ecotype E5 was higher in the period from January, 2007 to April, 2007, totaling 78,436 (77.7%) of the total specimens collected in this biotope. The Kruskal-Wallis ANOVA indicated a significant difference between the number of sand flies collected in this period and the previous (p = 0.007686) and subsequent periods (P = 0.000966) (Table 2). The sand flies were collected mostly (90.9%) from September, 2006 to April, 2007; during this period the total rainfall was 1,429.3 mm, compared to 683.3 mm in the remaining months (Table 2). The HM of sand flies collected in ecotypes E2, E4, E5, and E9 increased markedly during 2006/2007 in relation to the 2005–2006 period (Table 3). The species collected have been recorded previously in the Recanto Marista, with a predominance of Ny. neivai (Teodoro et al. 2001, Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008). The species Ny. neivai, Ny. whitmani, Mi. migonei, Pi. fischeri, and Pi. pessoai have been reported often in the Recanto Marista and elsewhere in the Paraná (Silva et al. 2008, Membrive et al. 2004, Teodoro et al. 2006). Ny. neivai, the most frequent species in Recanto Marista, has been found naturally infected by Leishmania (Córdoba-Lanús et al. 2006, Marcondes et al. 2009), including at the Recanto Marista (Oliveira et al. 2011). This species is anthropophilic, occurs in forests, adapts well to forest edges and modified environments, and may develop in the peridomicile and invade houses (Marcondes 2011). The second most frequent species in the Recanto, Ny. whitmani, was also observed to be naturally infected by Leishmania (Azevedo et al. 1990, Luz et al. 2000), is anthropophilic and adapts to forest environments, but tends to be scarce in deforested areas (Marcondes 2011). Peterson and Shaw (2003) suggested that Ny. whitmani might represent an example of high tolerance of an insect to drastic ecological changes, with its ability to survive and adapt to new ecological niches. In the eastern state of Santa Catarina, Ny. neivai predominated close to homes where cases of CL were reported (Marcondes et al. 2005). In this region the vegetation is much altered, which probably facilitated the adaptation of this species in areas close to houses (Marcondes et al. 2005). Thus, a new epidemiological profile of CL can result from environmental changes caused by humans, resulting in “a partial or complete domiciliation of some sand fly species” (Costa et al. 2007). Ny. neivai and Ny. whitmani show similar seasonal behavior; the population increase of these species coincides with the months of highest rainfall, as noted earlier, in this locality (Teodoro et al. 2007b, Reinhold-Castro et al. 2008). In ecotypes E2, E5, and E9, the hourly mean (HM) of sand flies collected in 2006/2007 increased markedly compared with the means for sand flies collected in 2005/2006. The increase in sand fly HM in the ecotype E2 was due to the presence of cattle and sheep that sheltered at night in a small shed next to E2 (hen house). The presence of these animals provides blood sources and an accumulation of organic matter (waste feed and animal feces) in the soil. It is thought that the sand fly increase in ecotype E5 was due to the organic waste removed from the hen houses that was used as fertilizer in the kitchen garden next to E5 in the period from January to April, 2007. During this period, 77.7% of the sand flies were collected from ecotype E5. It is important to emphasize that from July, 2006 to November, 2007, 35.1% of the total insects in ecotype E5 were collected, compared to 3.0% from the total previously observed (Teodoro et al. 2007b). This increase in the number of insects collected probably occurred because of the formation of breeding sites in the kitchen garden due to the deposition of organic matter in very moist soil. The disposal of waste in that kitchen garden was suspended in April as soon as this was discovered. In the following months, the number of insects collected in E5 decreased sharply. The growth of HM in ecotype E9 may have occurred because of inattention to cleanliness and the constant leakage of water in this biotope. In all three situations, the accumulation of organic matter (waste feed and animal feces) and the moist soil near the ecotypes may have favored the formation of sand fly breeding sites. The opposite situation was observed in ecotype E10 in several collections, i.e., a significant decrease in HM, which may have occurred as a consequence of the absence of chickens and lack of light. The proportion of sand flies (93.4%) collected in the hen-house ecotypes was significantly higher than in the other ecotypes. Previous studies in this locality found similar results, showing that the hen houses may be acting as zooprophylactic barriers, reducing the population of sand flies in the residences and in the lodge (Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008). However, cleaning the chicken yard is essential to prevent the formation of sand fly breeding sites in these environments in addition to other measures of environmental management (Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008). Alexander et al. (2002) mentioned that the shelters clearly offer important refuges for sand flies and an existing infection might be eliminated when sand flies take a second blood meal from the chickens. On the other hand, in experimental studies, chicken blood supported the development of Leishmania infections in sand flies (Nieves and Pimenta 2002, Sant'Anna 2010) as well as improving the development of the insect (Noguera et al. 2006). In the Recanto Marista, in addition to environmental management, chemical insecticides are sprayed on the buildings two to three times a year when the sand fly population has grown too much. Moreover, the windows and doors of domiciles are all screened. However, all these measures combined are not enough to prevent CL (Campbell-Lendrum et al. 2001), if the inhabitants of endemic areas fail to implement them fully. The use of residual insecticides requires improved knowledge of the vector's behavior, a public-health infrastructure with trained personnel, adequate equipment (Alexander and Maroli 2003, Maroli and Khoury 2006), and a commitment to maintain active entomological surveillance. The results of research in Paraná (Silva et al. 2008, Teodoro et al. 2003, Teodoro et al. 2007b, Reinhold-Castro et al. 2008) have shown that the actions taken by humans in the place where they live, even if subtle, determine the growth or reduction of the sand fly population in different microenvironments. Therefore, entomological studies should be performed in several endemic units, because when they are restricted to a few units in a very large area it is impossible to know the complexity and dynamism for each unit that make up the Leishmania transmission network (Teodoro et al. 2010, Teodoro et al. 2011). Studies of sand fly interaction with the environment have exposed some vulnerability of these endemic disease-bearing insects, allowing monitoring of the deployment of anti-sand fly measures and epidemiological surveillance, and can guide efforts to control theses insects more efficiently and effectively in areas where there is a transmission risk (Teodoro et al. 2010, Teodoro et al. 2011). One strategy to stop any vector-borne disease is to reduce human-vector contact, since the capacity of a vector to transmit pathogens is related to its density (Umakant and Sarman 2008). Thus, in a dynamic human-altered environment, the understanding of sand fly survival dynamics can contribute substantially to the prevention of CL. The decentralization model of health services adopted in Brazil has been a monumental failure, especially in the case of endemic vector-borne diseases where its actual effects have been negative. Hence the importance of reflecting on the words of Halstead (1988), that even in situations where resources for vector control are appropriate for the implementation of a program, they have often been unsuccessful, mainly due to five factors: the desire to find easier solutions, the loss of technical skills and managerial personnel, increase in the size of the problem, indifference to past experiences, and the expectation of failure, reflected in past unsuccessful experiences in controlling dengue and other vector-borne diseases. It is also necessary to reflect on the fact that “we are faced with a critical shortage of specialists trained to respond effectively to the resurgence of vector-borne diseases” and “adequately trained personnel are lacking in most developing countries, as are academic institutions with the programs to train them” (Gubler 1998). The Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (Process 410550/2006–0) provided financial support. We thank the Colégio Marista for permission to conduct the assessments and logistical support and João B. Kühl, technician of the Department of Basic Health Sciences of UEM, for instruction and aid in the identification of sand flies.