Dynamics and Characterization of Aedes aegypti (L.) (Diptera: Culicidae) Key Breeding Sites

Transcription

1 Neotrop Entomol DOI /s PUBLIC HEALTH Dynamics and Characterization of Aedes aegypti (L.) (Diptera: Culicidae) Key Breeding Sites MA VALENÇA 1,LSMARTEIS 2,3,LMSTEFFLER 3,AMSILVA 4, RLC SANTOS 3,5 1 Secretaria de Estado da Educação, Sergipe, Brasil 2 Fac de Saúde Pública, Univ de São Paulo, São Paulo, SP, Brasil 3 Depto de Morfologia, Centro de Ciências Biológicas e da Saúde, Univ Federal de Sergipe, São Cristovão, SE, Brasil 4 Depto de Medicina, Centro de Ciências Biológicas e da Saúde, Univ Federal de Sergipe, São Cristovão, SE, Brasil 5 Av. Marechal Rondon s/n Campus Univ Bairro Rosa Elze, São Cristóvão, SE, Brasil Keywords Dengue, epidemiology, insect surveillance, vector control Correspondence RLC Santos, Av. Marechal Rondon s/n Campus Univ Bairro Rosa Elze, São Cristóvão, SE, Brasil; rlacorte@ufs.br Edited by Neusa Hamada INPA Received 4 March 2012 and accepted 30 January 2013 * Sociedade Entomológica do Brasil 2013 Abstract The present study aimed to analyze the dynamics of containers used as breeding sites by Aedes aegypti (L.) in the city of Aracaju, SE, one of the Northeast Brazilian states. A total of three entomological surveys were performed during different precipitation levels. Breeding sites were categorized according to their function into storage, disposable containers, and reusable containers. Mean number of pupae and frequency of each type of breeding site were the criteria considered to identify key breeding sites. House index and Breteau index were calculated in each survey. A total of 3,647 water reservoirs were found, of which 220 were breeding sites, where 22,880 immature forms were identified. There were no differences in the mean number of larvae of several types of breeding sites and in the number of larvae among surveys. Larval indices showed a reduction in the second visit, but with no effect on adult occurrence when the number of pupae was considered. Key breeding sites resulted from containers used for water storage. The area studied showed conditions favorable to a new epidemic of dengue fever. Introduction Dengue fever is one of the most important arbovirus infections nowadays, particularly affecting countries with a tropical climate. In 2008, 585,769 cases of dengue fever were reported in Brazil, including 448 deaths. The northeastern region recorded 175,976 cases, with 69 deaths (SVS/MS 2011). According to the State Department of Health/Epidemiological Surveillance Center (CVE/SES), 25,703 cases of dengue fever were confirmed in the state of Sergipe, including 47 deaths. From these, 12,160 cases were confirmed in April, at the height of the dengue epidemic. In view of the complexity of dengue transmission and the lack of instruments to deal with this, disease prevention and control are aimed at the vector. Despite the broad distribution of Aedes (Stegomyia) albopictus (Skuse) in Brazil (Santos 2003, Martinset al 2006, Aguiaret al 2008, Honorio et al 2009), Aedes (Stegomyia) aegypti (L.) is the only confirmed vector in this country. Despite the existence of nationwide campaigns to raise the population awareness on the correct management of containers that are used as breeding sites for this mosquito, containers that serve as breeding sites are quite distinct from one region to another in Brazil and have a different role as they are associated with regional population habits (Lima et al 1998, Lefèvre et al 2004, Silva 2006, Medronhoet al 2009). Regardless of the control measures adopted, it is necessary to be clear about what types of containers are relevant in a certain area to establish vector control strategies, not only in terms of frequency, but also of productivity and persistence. In addition, to raise awareness on the

2 Valença et al importance of mosquito breeding sites, it is important to consider the relevance of each particular type of container on the everyday life of people in different regions, as this becomes a relevant factor in order to have the population engagedandtohaveasuccessful control strategy in use (Braga & Valle 2007). Breeding sites can have an aesthetic function, such as bromeliads, pots, and large containers with flowers, an economical role, such as tires, recyclable bottles, and cans, or play a role on survival, such as water reservoirs. In Brazil, the infestation indices used by the A. aegypti control program consider the presence of breeding sites of immature forms of the vector (Coelho et al 2008). However, surveillance based on the larval stage is not a good indicator of risk of transmission because it does not accurately show infestation by adult mosquitoes (Focks & Alexander 2006). Thus, aiming to focus on relevant containers where adult forms are produced, current studies have also considered the presence of pupae, as the occurrence of this stage of development is a better indicator of adult occurrence (Medronho et al 2009). This approach comes from studies on the productivity of breeding sites, which take the amount of pupae into consideration (Forattini et al 1997), although the current trend is to include the number of pupae exclusively, rather than the estimation of daily emergence of females as earlier recommended (Focks et al 1981, Focks & Alexander 2006). Thus, we aimed to study the dynamics of breeding sites of A. aegypti in a district of the city of Aracaju (SE), Brazil, and to identify the key breeding sites to support the development of effective control measures against this insect. Material and Methods Study area This study was performed in the district of Porto Dantas ( S, W), situated in the city of Aracaju, capital of the state of Sergipe, in the northeastern region of Brazil. Porto Dantas is geographically limited by a mangroveecosystem,thesergiperiverandthe Morro do Urubu an environmental protection area. According to the information from the Municipal Department of Health (personal communication), nearly 4% of the houses of the Porto Dantas district were infested by A. aegypti and there were no cases of dengue reported by the time we initiated our sampling. The city of Aracaju has a humid and subhumid megathermal climate, with mean annual precipitation of 1,590 mm and mean annual temperature of 26 C. The rainy season is between March and August (Prefeitura de Aracaju 2009). Data collection We conducted a total of three entomological surveys during periods with distinct precipitation levels and visited all properties in the district including stores, health clinics, and police stations for a quantitative and qualitative assessment of the existing breeding sites. All water containers that were not properly covered were considered to be water deposits, regardless of their use and the type of material they were made of. Water containers containing immatures of A. aegypti were considered breeding sites. Visits were conducted during working days and properties that had been closed during the week were visited on Saturdays. The first survey was conducted at the end of the rainy season, with a cumulative monthly precipitation of 63.1 mm (September 2007); the second one in the beginning of the following rainy season with a cumulative monthly precipitation of mm (February 2008); and the third one in the dry season, with a cumulative monthly precipitation of 17.7 mm (November/December 2008) (Fig 1). Data on rainfall were provided by the Secretaria de Estado de Meio Ambiente e Recursos Hídricos de Sergipe (SEMARTH 2011). Containers with accumulated water were quantified and classified according to their location (indoors or in the peridomicile area), exposure to sun (in shaded or sunny areas), and type of container (water tanks, barrels, laundry sinks, tires, metal cans and plastic containers, bottles, plant pots, water troughs, and others). These types of containers were separated according to their use as for storage, reusable, disposable, and others. Immatures of Culicidae were collected regardless of their stage of development and the water in the containers was subsequently discarded. Larvae and pupae were captured with the aid of flashlights, pipettes, and small fishing net according to the number of immatures and conditions of each container. When large water deposits were located, the material was collected with the small fishing net and placed in a basin with clean water. Pupae were separated from larvae, counted, and subsequently stored in plastic cups. All samples collected were taken to the laboratory for counting and identification. Data analysis The data obtained from the three surveys were validated and analyzed using the EpiInfo and SPSS version 15.0 software programs. House index (percentage of houses infested with larvae or pupae) and Breteau index (number of positive containers per 100 houses inspected) were calculated for the Porto Dantas district in each survey. The mean number of larvae and pupae for each functional category and the number of immatures per breeding site and per property were calculated to analyze the dynamics of containers used as breeding sites for A. aegypti.

3 Aedes aegypti Breeding Sites Fig 1 Monthly precipitation in Aracaju (SE), Brazil, between January 2007 and December Arrows show survey periods. HI house index, BI Breteau index. Data followed a non-gaussian distribution and were subjected to the nonparametric Kruskal Wallis test, followed by Mann Whitney test to compare samples two-by-two. The number of pupae and frequency of the different types of breeding sites were the criteria considered for the identification of key breeding sites. Results A total of 3,647 water containers were found in the district of Porto Dantas during our surveys. Of these containers, 220 were breeding sites of A. aegypti, and 22,880 immatures were collected (Table 1), with the majority being located in the peridomicile area (92.8%). The number of breeding sites and, consequently, the larval indices decreased throughout the surveys (Fig 1), although the number of containers with water remained high (Table 2). In addition to A. aegypti, only immatures of Culex quinquefasciatus (Say) were observed. Laundry sinks, an unusual way to store water (Fig 2), were the most frequent breeding site for this mosquito in the area, totaling 67.1% of all breeding sites in the beginning of the rainy season. Tires were the second most frequent breeding site in our first survey at the end of the rainy season, but were less frequent in the two subsequent surveys. Potted plants were uncommon breeding sites, although they became relatively important when the total number of breeding sites was reduced during the dry season. The number of breeding sites decreased from 130 in the first survey to 76 in the second survey (the end of the rainy season and beginning of the following rainy season). This decrease in the number of breeding sites was accompanied by a reduction in the number of larvae, dropping from 12,929 to 7,985 larvae, with (first survey) to 7.57 (second survey) larvae per property in average (P<0.05). However, the number of pupae was similar in both surveys, with an average of 0.49 and 0.48 pupae/property, respectively (P=0.54) (Tables 1 and 2). Table 1 Distribution of immature forms according to type of breeding site (Porto Dantas, Aracaju, Brazil, 2007/2008). September 2007 (end of the rainy season) February 2008 (beginning of the rainy season) November 2008 (dry season) Containers Amount/ frequency (%) Larvae Pupae Amount/ frequency (%) Larvae Pupae Amount/ frequency (%) Larvae Pupae Total of immature forms Cement laundry 67/51.6 5, / / ,762 sink Water tank 5/3.8 2, / / ,332 Barrel 11/ / / ,560 Tire 16/12.3 2, / / ,648 Can/plastic 9/ / / container Bottle 9/7.0 1, / / ,071 Flower pot 5/ / / Water trough 0/ / / Others 8/ / / Total 130/ , / , / ,880

4 Valença et al Table 2 Amount of households and availability of containers with water in the three surveys (Porto Dantas, Aracaju, Brazil, 2007/2008). September 2007 (end of the rainy season) February 2008 (beginning of the rainy season) November 2008 (dry season) Total number 1,094 1,134 1,164 of households Households 853 (78) 863 (76.1) 821 (70.5) visited (%) Containers 1,334 1,235 1,078 with water Breeding sites Larvae/breeding sites Larvae/property Pupae/breeding sites Pupae/property The mean number of larvae did not differ among the several types of breeding sites (minimum value, 48.4 larvae per plant pot; maximum value, per water tank; P> 0.05). Nonetheless, the mean number of pupae was systematically lower in bottles when compared to the remaining breeding sites (tires, P=0.01; water tank, P=0.03; metal cans and plastic containers, P=0.03; laundry sink, P=0.07; barrel, P=0.05). In addition to bottles, plant pots also showed a trend towards producing a lower number of pupae (tires, P=0.02; water tank, P=0.07). When the analysis was performed per functional category, no statistical differences were observed in the number of larvae among surveys and per category. However, the number of pupae varied among surveys and among functional categories (P=0.024), with the highest number being found in the disposable containers and the lowest in the reusable ones. When stratified per survey, the highest mean (10.0) was observed among disposable containers and the lowest among reusable containers in the first Fig 2 Cement laundry sink used as a water reservoir, the main breeding site in the study area, Aracaju, survey (P=0.0045). The average number of pupae in the second survey (P=0.24) did not differ among containers. In the third survey, disposable containers were negative and the others did not show significant difference in the mean number of pupae recorded (Table 3). Discussion Aedes aegypti is one of the mosquito species showing the highest levels of synanthropy and anthropophily. The entire biological cycle is completed in the domicile and peridomicile where hosts and resting and oviposition sites are commonly available. Our surveys indicated the peridomicile as the environment with the highest number of breeding sites, although water containers (plant pots, storage buckets, broken toilet water cisterns, and others) were available inside properties, as similarly reported elsewhere (Donalísio & Glasser 2002, Silva et al 2006). Nonetheless, in the present study, the constant presence of breeding sites in the peridomicile area was mainly associated with the availability of containers used for water storage, such as laundry sinks. The shape of these sinks facilitates the retention of water in which larvae could be collected. This type of sink is made of plain cement, so that their lateral walls are suitable surfaces for oviposition. In addition, they are usually situated in shaded areas, have no lid, and their water is not replaced during long periods of time, thus promoting the maintenance of the mosquito cycle, even in the dry season. Other studies have reported similar information about the role of water storage as breeding sites in areas with deficiency in water supply (Arredondo-Jimenez & Valdez-Delgado 2006, Medronho et al 2009, Chadee et al 2009, Villegas-Trejo et al 2011). The reduction in the frequency of breeding sites observed during the course of our surveys could have been caused by human and/or natural factors. The research intervention itself could be described as an anthropogenic factor, as the water accumulated in the located containers was always discarded upon the residents authorization. Another measure that certainly contributed to decreased frequency in breeding sites observed was the more active campaign promoted by health agents to control mosquitoes as a consequence of the dengue fever epidemic that occurred in 2008 in Sergipe. The lower precipitation observed during the second and third surveys could also have led to the decrease in the number of breeding sites in disposable containers. However, the great number of containers with water that were available during our surveys diverges from the role of precipitation in the reduction in the number of breeding sites and, consequently, infestation indices. If, on the one hand, the lack of rain keeps all disposable containers and some of the reusable containers

5 Aedes aegypti Breeding Sites Table 3 Frequency and mean of larvae (ML) and pupae (MP) according to container functional category (Porto Dantas, Aracaju, Brazil, 2007/ 2008). Categories September 2007 (end of the rainy season) February 2008 (beginning of the rainy season) November 2008 (dry season) % ML MP % ML MP % ML MP Storage Reusable Disposable Others Total dry, on the other hand, the population tends to store water for longer periods of time during the dry season. When precipitation was taken into consideration in the first survey, which was performed after the rainy season, the highest number of breeding sites and immature forms was recorded. In the second and third surveys, performed after the decrease in precipitation, fewer breeding sites were found, especially those in the disposable and reusable container categories. The reduction in the number of breeding sites was not closely associated with productivity, compared to the first and second surveys, when the mean number of pupae per breeding site practically doubled, despite the decreased number of breeding sites. Among the possible explanations for the increase in the relative number of pupae are the non-overflowing of breeding sites due to a reduction or absence of precipitation and the lower frequency of replacement of water in the laundry sinks due to its scarcity. The importance of plant pots, bottles, and even egg shells and bottle caps is emphasized in governmental campaigns, but an increasing number of studies have shown the importance of large storage containers to the infestation of properties (Forattini & Brito 2003, Chadee et al 2009, Medronho et al 2009, Monteiro et al 2009, Villegas- Trejo et al 2011). Laundry sinks and water tanks were considered the key breeding sites when the frequency and the mean number of pupae were considered. These containers successfully allowed for the full development of mosquitoes and were spread throughout the entire district. Despite the relevance of storage containers, several times, the material distributed to inform people about mosquito breeding sites follows national standards, not emphasizing or omitting the importance of these types of regional breeding sites among the illustrations shown (Marteis et al 2011). According to the observations made in this study, the general reduction in larval indices had no apparent effect on the production of adult mosquitoes when the number of pupae is considered. This shows that depending on the index considered, the risk of dengue transmission could result in different estimates. In this case, the maintenance of pupae production could have occurred due to the favorable conditions for immature forms to complete their cycle of development in storage containers and to reach the adult stage. These favorable conditions may have resulted from the less frequent replacement of water in the reservoirs during the dry season. Thus, the decreasing in the number of breeding sites led to a reduction of the total population of immature forms, but otherwise, the lack in the water supply promoted more stability in storage containers and maintained the production of adults. Our study reinforces what has been observed in other endemic areas of dengue fever that has been led to paradigm shift in relation to the infestation indices, suggesting pupal surveys as first choice of data source for developing target strategy and transmission risk assessment (Focks & Alexander 2006, Garelli et al 2009). Consequently, the vector control strategies would be redirected, being aimed at the control of large reservoirs. Accordingly, recent studies have reported a great short-term reduction in the population of adult mosquitoes when water storage reservoirs, identified as key containers in an area, were covered (Maciel-de-Freitas & Lourenço-de-Oliveira 2011). In addition, the cost of reducing only key containers is lower, but it has been demonstrated to be as efficient as trying to reduce all containers (Tun-Lin et al 2009). The reduction in the number of breeding sites and, consequently, in the larval indices does not imply in the absence of the risk of dengue transmission in the face of a high number of containers available even in the dry season that could potentially become new breeding sites for A. aegypti (Table 2). The current production of adult mosquitoes associated with the large number of containers would be enough for mosquitoes to spread throughout the area again in a short period of time and contributing to a new dengue fever epidemic (Marteis et al 2013). Our data demonstrated the importance of considering the number of pupae present in breeding sites for the transmission risk assessment and that in spite of a great diversity of containers can be used as breeding sites for A. aegypti, some unusual types may have high local relevance. Storing water in

6 Valença et al laundry sinks has already been reported in Mexico (Arredondo- Jimenez & Valdez-Delgado 2006), and similarly to our observations, at least one laundry sink was present in almost 100% of households, which was also one of the main issues for pupal production. It has been suggested that the local adult populations of A. aegypti under such conditions could probably be reduced by concentrating anti-larval measures for the management on key breeding sites. The report of unusual breeding sites indicates the need for further studies to identify the key containers which should be the focus of surveillance to better target and efficiently prevent dengue epidemics. Likewise, it is unlikely that solutions centrally produced, such as the federal campaigns, would contemplate the variety of containers available in different regions and regional, educational approaches and campaigns should be encouraged. 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