Background
Approximately 6.01 billion people currently live in areas suitable for
Aedes aegypti disease transmission [
1].
Ae. aegypti-borne diseases, such as dengue (DENV), chikungunya (CHIKV), and Zika (ZIKV) viruses, are found in tropical and subtropical zones with an abundance of these species, including Central America [
2‐
4]. Other than for yellow fever vaccine [
5], no broadly licensed commercial vaccines are available for the principal
Ae. aegypti-borne arboviruses, so vector control remains the primary strategy to limit their spread [
6]. Climate change, urbanization, migration, human behavior, and ecosystem modification are among the myriad factors influencing the geographic spread of
Ae. aegypti and their associated viruses [
1,
7,
8].
Ae. aegypti are highly productive in urban environments and have a strong preference for human blood [
9].
Ae. aegypti spend the majority of their lives in the houses where they emerged, flying an average of 40–80 m during the course of their lifetimes [
10]. Oviposition sites are selected based on their physical, chemical, and biological characteristics, such as container type, depth, water quality, and sun exposure [
11,
12]. Ideal larval habitats for
Ae. aegypti are dark-colored containers filled with stagnant water and organic material in shaded areas around houses [
11,
13,
14]. Productive container types include flower pots, tires, vases, buckets, cans, rain gutters, fountains, bottles, and birdbaths [
11,
13,
14]. Greater human population densities provide more feeding opportunities for
Ae. aegypti [
15]
.
Studies of socioeconomic status (SES) impacts on
Ae. aegypti abundance mostly report greater
Ae. aegypti population densities in low SES areas [
16‐
22]. Most studies have only considered income, occupation, and education as the SES factors. Few studies have evaluated associations between household environmental measures as attributes of SES and mosquito abundance. The household environmental factors that can influence mosquito infestation are quite heterogeneous. These include piles of garbage [
21], open wells [
23,
24], storm sewers [
25], and septic tanks [
26]. Less information is available on spatial risk factors, but proximity to vacant lots [
27,
28], vegetation or green spaces [
29], other houses/structures [
30], and roads [
31,
32], have been shown to be predictive of mosquito abundance. Household infrastructure may also influence the mosquito microenvironment [
33‐
35]. For example, the
premise condition index has been shown to be an effective tool at classifying houses according to risk of having mosquito breeding sites [
33‐
35]. This index can be used to prioritize neighborhoods for vector control interventions.
For this study, we evaluated whether proximity to other houses/structures and roads, and household environmental factors were associated with immature mosquito abundance. A secondary objective was to determine how mosquito abatement interventions, including fumigation and cleaning possible larval habitat containers, influence immature mosquito abundance. It is particularly important to examine these relationships in Central America, which has been host to large outbreaks of arbovirus infection and where vector control resources are limited [
36].
Discussion
This study identified environmental factors and SES attributes that were associated with mosquito larvae and pupae abundance. Distance to the nearest paved road and house/structure were inversely associated with larvae and pupae abundance and were significant mediators of the relationship between environmental capital and the number of larvae and pupae per house. Cubic splines revealed that households of middle environmental capital had significantly more larvae and pupae than those with the lowest and highest environmental capital.
Our finding that households closer to paved roads had more larvae and pupae is consistent with previous studies from Kansas and Bermuda, which found greater numbers of adult mosquitoes and eggs closer to roads [
31,
32]. Proximity to paved roads may indicate greater population density, which would include more containers and greater availability of blood meals. The association remained significant after adjusting for the total number of containers ≥3 L per household, which may suggest a greater presence of smaller containers like cups, cans, and bottles, in areas closer to roads [
31]. These containers are also conceivably productive larval habitats. This association was further supported by mediation analyses, which showed that distance to the nearest paved road was a significant mediator of the relationship between environmental capital and number of larvae and pupae. As environmental capital increased, distance to the nearest paved road decreased. Households closer to paved roads had significantly more larvae and pupae, holding environmental capital constant. It is conceivable that households with greater environmental capital, which are closer to roads, are more likely to own barrels and other large water storage containers, which may support larger mosquito populations if they are not properly managed. More mosquitoes in areas closer to paved roads may also increase the risk of the spread of arboviral infections, which was reported in a CHIKV study in Pakistan [
63].
Distance to the nearest highway was not a significant predictor of larvae and pupae abundance. One study in Taiwan reported that the number of dengue fever cases corresponded inversely with distance from highways, further indicating that
Ae. aegypti abundance may be associated with population density [
64]. Proximity to highways in our study was not necessarily suggestive of greater human population density, which may have greater influence on mosquito abundance [
65,
66]. These results may suggest that the immediate household environment contributes more to larvae and pupae abundance than more distant neighborhood factors [
67‐
69]. This is particularly important for
Ae. aegypti, as immatures tend to be highly aggregated in space and time, rarely dispersing beyond 30–40 m of the household where they developed as larvae [
67,
69].
Distance to the nearest house/structure was inversely associated with larvae and pupae abundance. Furthermore, mediation analyses revealed that households with higher environmental capital were closer to other houses/structures and had significantly more larvae and pupae. We are unaware of other studies assessing distance to the nearest structure as a mediator between SES and mosquito abundance. Previous studies of associations between distance to the nearest building and mosquito abundance are inconsistent. Some report greater
Anopheles and
Aedes abundance in houses/structures closer together [
30,
70,
71], whereas others do not [
31,
72]. Urbanization and greater human population density lead to a greater number of artificial containers, which creates an abundance of potential habitats for mosquitoes, including tires, flowerpots, and cans [
15]. Urban environments may also be more favorable for
Ae. aegypti due to the absence of natural vegetation, competition, and predation [
12,
15,
73,
74]. These results reinforce the premise that mosquito control requires community-wide efforts, as individual houses with disproportionately high numbers of mosquitoes may pose risks to their closest neighbors, and indeed the entire community [
68].
Recent history of fumigation inside/outside of the house and containers that had been cleaned but could still serve as immature habitats for mosquitoes were not significant mediators between environmental capital and the number of larvae and pupae. Fumigating and cleaning containers with standing water are established mosquito control measures [
55,
56,
75]. Fumigation is only provided by MSPAS in Guatemala. It could be that our measure of environmental capital was not predictive of these preventive measures in these communities or that fumigation may not have been effective in these areas. Alternatively, our cross-sectional survey that asked whether participants performed these prevention measures in the last 6 months may have been insufficient to assess the efficacy of these interventions, which require repeated application. Fumigation frequency and insecticide resistance should be also considered.
Households of middle environmental capital had significantly more larvae and pupae than households with the lowest and highest environmental capital for both surveys. In this study, environmental capital included access to running water, improved sanitation, a sewer system, and trash disposal service, which are typically associated with reduced mosquito populations [
23,
24,
52,
76‐
78]. Greater environmental capital may also indicate higher values of other SES indicators, including income, occupation, and education, which are associated with greater mosquito prevention measures, such as removing containers with standing water [
17‐
19,
21]. Conversely, low environmental capital was associated with greater distance to the nearest paved road, which was associated with fewer mosquitoes. It is conceivable that these distances exceeded the typical flight range for mosquitoes [
79]. Moreover, houses with low environmental capital in this study had fewer barrels and other large water storage containers that were most productive for mosquitoes.
Our study did not characterize larval genus or species, but multiple species of
Aedes,
Anopheles, and
Culex mosquitoes have been reported in Quetzaltenango department, where our study was conducted [
80‐
83]. Specific species in Quetzaltenango include
Ae. aegypti and
Ae. albopictus [
80,
81], which preferentially lay eggs in household containers [
84];
An. hectoris, An. parapunctipennis, and
An. xelajuensis, which prefer marshes, trees, swamps, fields, streams, and rivers [
85]; and
Cx. corniger, Cx. peus, and
Cx. quinquefasciatus, whose breeding sites include storm sewers, cesspits, and polluted water [
26,
86]. Given our container surveys occurred exclusively in households, we suspect that the majority of the immatures that we collected were either
Ae. aegypti or
Ae. albopictus.
Our study had several limitations. First, we sampled communities based on high entomological indices and are thus these are not representative of all communities in Guatemala. However, the households are representative of the local communities. Second, cross-sectional surveys of mosquitoes are time sensitive [
41] and our two surveys points were insufficient to fully capture the temporal variability of mosquito larvae and pupae, despite including both dry and rainy seasons. Third, our survey assessments of whether participants fumigated inside/outside the house or cleaned their containers in the last 6 months were likely inadequate to assess the efficacy of these prevention strategies. Fourth, we did not include containers < 3 L on household premises such as discarded cups and cans, which could also serve as immature mosquito habitats.
Acknowledgements
The authors are grateful to Dra. Beatriz Santamarina, Dra. Analuisa Castro de Quan, Juan López, Juventino Cobon, Negly Castillo, Jorge Sincal, Nazario López, Jorge Luis López Díaz, Carlos Enrique Vásquez Ramos, and Jonathan Josue López Barrios, as well as local authorities, vector control personnel, and all field staff from both Coatepeque and Génova.
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