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Spatial Stability of Adult Aedes aegypti Populations
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Publication date PMC-release:
01 December 2011
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Abstract
Vector control programs could be more efficient by identifying the location of highly productive sites of Aedes aegypti. This study explored if the number of female adults of Ae. aegypti in BG-Sentinel traps was clustered and if their spatial distribution changed in time in two neighborhoods in San Juan, Puerto Rico. Traps were uniformly distributed across each neighborhood (130 m from each other), and samples were taken every 3 weeks. Global and local spatial autocorrelations were explored. Spatial stability existed if the rank order of trap captures was kept in time. There was lack of global autocorrelation in both neighborhoods, precluding their stratification for control purposes. Hot and cold spots were identified, revealing the highly focal nature of Ae. aegypti. There was significant spatial stability throughout the study in both locations. The consistency in trap productivity in time could be used to increase the effectiveness of vector and dengue control programs.
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Most cited references33
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Heterogeneities in the transmission of infectious agents: implications for the design of control programs.
M. E. Woolhouse, C. Dye, J F Etard … (1997)
From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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Spatial and Temporal Clustering of Dengue Virus Transmission in Thai Villages
Introduction Dengue is the leading cause of human arboviral disease worldwide. Dengue viruses (DENV) of the family Flaviviridae and genus Flavivirus, co-circulate as four antigenically related serotypes (DENV-1, −2, −3, and −4), each in varying annual frequencies in Thailand [1] and other tropical countries. The container-breeding mosquito Aedes aegypti (L.) serves as the primary vector responsible for DENV transmission within human populations. Females feed preferentially and frequently on human blood and consequently live in and around human dwellings [2,3]. Transmission of DENV to humans results in either inapparent infection, undifferentiated febrile illness, dengue fever (DF), or life-threatening dengue hemorrhagic fever (DHF). Except for a few notable exceptions, vector control (larvicide treatments, insecticide sprays, and source reduction) has been ineffectively implemented, and no vaccine or clinical cure is yet available for use. Consequently, DENV remain a major cause of morbidity in the tropics and threaten to further expand geographically. DENV transmission and disease are determined by a combination of factors [4] involving the human host [5–7], virus [8–11], mosquito vector [12,13], and environment [13]. Although past studies have revealed general temporal and spatial patterns in the distribution and abundance of Ae. aegypti and human DENV infections [14–18], greater resolution of transmission dynamics across finer geographic and temporal scales is needed to refine current dengue surveillance and control strategies. In an earlier prospective cohort study of schoolchildren in Thailand, Endy and others [19] reported a nonuniform distribution of DENV illness and viral serotypes. To test the hypothesis that DENV transmission is spatially and temporally focal, we extended the school-based study design to include cluster investigations [20] in villages associated with schools. By sampling children and mosquitoes within the neighborhood of children absent from school with fever and dengue viremia, we hypothesized that we would be able to detect, in the same general area and time, other human and mosquito infections and more precisely identify determinants of transmission risk. We used school-based dengue cases to trigger village surveillance of children and mosquitoes within spatial and temporal clusters. We sought a rigorous study of cluster areas over a 15-d period to more accurately define the burden of DENV within a prescribed area (both inapparent and symptomatic infections) and its relationship to mosquito density and infectivity. On the basis of our data, we aimed to consider implications on improving disease prevention strategies. Methods Study Area and Selection of Schools and Villages Our study area (Muang District, Kamphaeng Phet Province [KPP], north-central Thailand [19]) is, by Thai standards, relatively sparsely populated with 233,033 residents in 63,500 houses in an area encompassing 1,962 km2. The average temperature is 28.0 °C with an average monthly rainfall of approximately 200 mm during the rainy months of May to October (National Statistical Office). We selected 11 participating primary schools on the basis of higher numbers of hospitalized dengue cases amongst their students during the prior 5 y, proximity to our field station, and interest of the school administrators. Selected schools (Figure 1) were associated with 32 villages (8,445 houses). Given the workload limitations of entomological surveys, 20 of these villages (4,685 houses) were selected for inclusion on the basis of the density of houses, favoring those with houses in close proximity of each other ( 20–40 m, >40–60 m, >60–80 m, and >80–100 m). In order to evaluate for a distance effect in conjunction with enrollee demographics, a multivariate logistic regression model was formulated. Scientific and Ethical Review and Approval The study protocol and consent forms were approved by the AFRIMS Scientific Review Committee and the ethical review committees of the U.S. Army Surgeon General, Thai MoPH, University of California at Davis, University of Massachusetts Medical School, and San Diego State University. Results Initiation of Cluster Investigations Of the 1,204 febrile children (506 in 2004 and 698 in 2005) who provided blood specimens, 48 (28 in 2004 and 20 in 2005) had detectable DENV viremia. Thirty-four cluster investigations were conducted during the study period (Table 2). Ten clusters (five pairs) in 2004 and two clusters (one pair) in 2005 were spatially and temporally matched. The sex and age distribution of the positive and negative index cases were similar. Children in 58% (seven of 12) of the positive clusters (six in 2004 and one in 2005) attended a single school (school number 2). Table 2 Summary of Cluster Investigations Cluster Enrollees Among the 556 village enrollees (217 in positive and 339 in negative clusters), 27 DENV infections were detected during the 15-d follow-up period. These incident infections occurred exclusively in positive clusters (t-test; p < 0.01; AR = 10.4 per 100; 95% confidence interval [CI] 1–19.8 per 100). This result represented a 4.9% risk among enrollees for experiencing a DENV infection within 15 d of cluster initiation, but a 12.4% risk among enrollees who resided in a positive cluster. Cluster number 4 (Figure 2) contributed disproportionately to this difference. However, all but one positive cluster (cluster number 12) exhibited at least one neighbor with dengue within the 15-d period. There was a statistically significant clustering of DENV cases close to the center of positive clusters when we examined all positive clusters together (Figure 3). Demographics of enrollees between positive and negative clusters were comparable (Table 3). There was no difference in distance between the index cases and respective enrollees in the positive and the negative clusters. Table 3 Comparison of Dengue-Positive and Dengue-Negative Clusters Figure 2 Intense DENV Transmission in Cluster 4 Cluster number 4 illustrates extensive DENV transmission occurring within a 15-d period. In comparison, the paired negative cluster (cluster number 5, not shown) included 22 houses, 21 Ae. aegypti, and 15 contacts with no evidence of DENV transmission within a 15-d period. These index cases were 258 m apart and the cluster investigations were initiated 2 d apart. Figure 3 Clustering of DENV Infections within Positive Clusters This graph shows the relationship of distance between the houses of enrollees and the index case in the positive clusters and the proportion of those enrollees that experienced DENV seroconversion. Error bars represent 95% CIs of the proportions. Numbers in parenthesis indicate the number of positive enrollees and the total number of enrollees in each distance interval. The relationship between distance and the proportion of enrollees that are dengue positive was significant (Fisher's exact test, p < 0.001). A multivariate logistic regression model was estimated to examine the focal nature of transmission while controlling for cluster demographics. Distance between the house of each enrollee and the index case was the measure of focality. An indicator variable was used to account for the evidently excessive transmission in cluster number 4. The model included the age and gender of the enrollees as well as the interaction of these two variables. Resulting coefficient estimates, standard errors, and p-values are given in Table 4. A diagnostic test does not indicate a lack of fit (Hosmer-Lemeshow test, p = 0.23) [30]. A negative and significant parameter estimate indicated that the probability of infection decreased as the distance between enrollees and the index house increased. Modeling results also indicate a gender difference in the effect of age on the probability of infection. The probability that a male enrollee seroconverted decreased with age. This effect was not observed among female enrollees, in whom older enrollees had a higher probability of infection. These trends are apparent in the distribution of infections (Figure S1; Table 5). Table 4 Results of Multivariate Logistic Regression Analysis Table 5 Infections among Enrollees in Positive Clusters by Gender and Age Group Clustering was additionally observed within households as has been previously described [31]. Relative risk of dengue seroconversion among household enrollees of a dengue versus non-dengue case was 2.63 (95% CI 0.96–7.21; Pearson's Chi2 test) with an absolute risk of 6.88 per 100 (95% CI 0–17.29), indicating a strong, but not statistically significant trend towards household risk. Of the 27 DENV infections among village enrollees (Table 6), 14 were inapparent, and 13 were symptomatic. Inapparent infections were more likely with primary (five out of six) than secondary (seven out of 19) DENV infections (p = 0.05; Pearson's Chi2 test). All but one positive cluster (cluster number 6) had concordance of serotypes between the index case and viremic enrollees. (Pearson's Chi2 test used.) Table 6 Clinical Spectrum of Illness among 27 Enrollees with DENV Infections Environmental Determinants of Transmission Among environmental features evaluated ( Table 3), positive clusters were less likely to have piped water than were negative clusters. Though the number of water-holding containers was similar in houses with and without piped water (17.6 ± 8.6 versus 17.8 ± 8.1, t-test, p = 0.28), containers with Ae. aegypti larvae or pupae were significantly less abundant in houses with than without piped water (3.2 ± 3.0 versus 4.4 ± 3.3, t-test, p < 0.001). Use of the larvicide Temephos was higher in the schools than in the villages; 43% and 30% of containers had Temephos in schools in 2004 and 2005, respectively. On average 10% of containers had Temephos in the villages during both study years. Mosquito Collections and Spraying A total of 1,022 adult female Ae. aegypti were collected from within and immediately surrounding homes (Figure 1; Table 2) of which eight (0.8%) were PCR-positive. The average proportion of houses sampled was 0.92 in the positive clusters and 0.93 in the negative clusters (t-test, p = 0.53). Average number of Ae. aegypti pupae/person was significantly higher in positive clusters (Table 3). Although no significant differences were detected, all classical entomological indices (House, Container, and Breteau) and average number of female Ae. aegypti adults/person were higher in positive clusters. The average proportion of houses sprayed was 0.87 in the positive clusters and 0.84 in the negative clusters (t-test, p = 0.39). A total of eight female Ae. aegypti were collected from schools associated with cluster initiation; none were PCR-positive. Discussion Although focal DENV transmission has been noted previously [14,15,32], to our knowledge this is the first study to demonstrate, using control clusters and precise human and entomological data, recent DENV transmission that was focal through space and over a short time span (15 d). DENV-infected hosts (27 enrollees) and vectors (eight Ae. aegypti) were exclusively identified in the 12 dengue-positive clusters, despite a nearly 1:2 ratio of enrollees between positive and negative clusters. Furthermore, we observed significant central clustering of DENV cases within positive clusters. We suspect that focal transmission was associated with recent DENV introductions because of the 217 paired serologic specimens from positive cluster enrollees, only one revealed an elevated but declining immunoglobulin M level, which would be indicative of a recent DENV infection occurring up to 60 d prior to cluster initiation [22]. Consequently, we attributed the observed DENV transmission (enrollees with viremia on day 0 or 15 and/or seroconversion between days 0 and 15) to recent virus introductions. This conclusion is in contrast, however, to data published by Beckett and others [20] who conducted cluster investigations in West Jakarta, Indonesia. They detected 175 recent DENV infections upon enrollment in 53 positive clusters compared to our one in 12 positive clusters, arguing against recent virus introduction. We attribute these contrasting results to study design differences. First, we recruited from schools whereas Beckett recruited from a hospital, potentially after the virus had undergone significant community-based amplification. Second, we preferentially enrolled children as the primary susceptible and amplifying portion of the host population. Beckett additionally enrolled adults. Adults may have exhibited greater background dengue immunity that may have confounded the serologic data. Third, Beckett's study was conducted in an urban area, in contrast to rural villages in our study. Differences in transmission dynamics between these kinds of habitats were likely shaped by the frequency of DENV introductions and diversity in human behaviors. Previous studies have documented hyperendemicity of all four DENV serotypes with an approximate 5% annual risk of acquiring an infection in KPP [19]. In our study, cluster number 4 had a 52% attack rate among enrollees sampled during the 15-d follow-up period. However, after excluding this cluster and its matched negative cluster, the adjusted AR remained high (six per 100). This number represented a 12.4% risk of an enrolled child acquiring a DENV infection within a 15-d period when living within 100 m of a child ill with dengue. Eleven of 12 positive clusters had at least one enrollee with acute dengue in addition to the index case. Given the required intrinsic incubation period, and the finding that all eight virus isolates from mosquitoes matched the serotype recovered from the index case suggest, though not definitively, that except for children from whom virus was recovered on day 15, multiple viremic children within a cluster were infected by one or very few infected mosquitoes. Other evidence within our study to further support village- and not school-based vector sources of DENV infection are that: (1) mosquito populations in schools were extremely low, (2) children seroconverting to dengue within a cluster attended different classrooms within the school, (3) genomic sequences of the envelope (E)-regions of the viruses isolated from children and mosquitoes within the same villages were identical (R.G. Jarman, unpublished data), and (4) housemates of dengue seroconverters had a higher relative risk for DENV infection than those of nondengue seroconverters. The latter observation is consistent with previous reports [14–16]. We suspect that the predominance of DENV transmission in KPP villages reflects, at least in part, routine and effective vector control in schools (insecticide every May and July and Temephos to containers every 3 mo), but not in village homes. Differences in transmission observed between positive and negative clusters could not be attributed to differences in enrollee demographics. Differences in behavioral factors, however, could not be excluded. Within positive clusters, risk of infection decreased with age for males and increased with age for females. This observation merits further investigation with a larger sample and analysis of sex-specific behaviors that might modify risk of infection with advancing age. The only statistically significant determinant among environmental features associated with focal DENV transmission was the greater availability of piped water in negative clusters. Though one may consider a causal relationship (that is, less piped water availability leading to greater need for water storage leading to more containers for larval mosquito development resulting in higher dengue risk), we found no difference in the number of containers between cluster types. Although accurate data on water turn-over are difficult to obtain, the greater number of positive containers in positive than in negative clusters could not be explained by a difference in the frequency of container turn-over rates that we measured. These data could reflect a historical norm or behavior in response to lack of reliability of piped water possibly guided by people's knowledge of dengue preventive measures [33]. The only statistically significant difference among entomological indices was the greater number of Ae. aegypti pupae per person in positive than negative clusters. It is important to note that observed mean pupae per person exceed by an order of magnitude the minimum entomological threshold estimated by Focks and others [34] for a different region of Thailand. This implies that even when pupal densities are relatively high, differences in this measure of entomological risk can be epidemiologically informative. Although adult mosquito population density tended to be higher in positive clusters, differences were not statistically significant, perhaps due to limitations in sampling adult Ae. aegypti with backpack aspirators. Alternatively, mosquito density may be most informative when viewed in concert with herd immunity, and mosquito density alone may be less relevant than the presence of DENV-infected mosquitoes that potentially can transmit virus to multiple individuals [2,3]. Dengue cases in enrollees occurred over a wide range of female Ae. aegypti densities (Figure 4). At densities higher than approximately 1.5 Ae. aegypti females per child, clusters were more likely to be positive than negative. This indicates that DENV transmission was more likely to occur at higher vector densities. Figure 4 Relationship between Vector Density and Dengue Cases Relationship between the number of Ae. aegypti females per child and dengue transmission within 12 positive and 22 negative cluster investigations in 2004 and 2005. Dengue transmission is expressed as the number of positive PCRs on days 0 or 15 of study or of dengue seroconversions between days 0 and 15 per child per cluster. Perifocal spraying is a common approach by health departments to contain/control dengue. However, this practice has been found to be ineffective in aborting DENV transmission [13,35]. Our data suggest that if school-based surveillance can be bolstered by rapid, easy-to-use, and affordable diagnostics, spatially and temporally focused vector control in rural areas such as KPP could be more effectively applied to contain new virus introductions and offset the theoretical risk of longitudinal transmission within and beyond village foci. Although the risk of infection decreased significantly with distance from the center of a cluster, we did not examine people living beyond 100 m of an index case. Our study did not define the spatial dimensions of DENV transmission. Nevertheless, we expect that interventions will need to go beyond a 100 m radius of the home of a DENV-infected child because viremic residents or visitors bitten by an infected mosquito can move virus farther than a flying, infected adult female Ae. aegypti [13,35]. We do not know the longitudinal effects of killing adult mosquitoes on transmission within a community. Koenraadt and others [27] determined in our study area that within 1 wk of spraying insecticide inside homes, approximately 50% of prespraying levels of Ae. aegypti populations were reestablished. Identifying only two of 217 child enrollees with dengue viremia on day 15, both approximately 50 m from the index case within the same positive cluster, indicates that vector control can be locally successful when promptly and properly applied in response to a dengue case. Insecticide applications are most effective when applied inside homes where most Ae. aegypti rest [12] and otherwise avoid contact with insecticides applied outdoors [35–37]. Though our study design was rigorous, our conclusions must be considered in the context of largely logistical limitations: (1) We did not sample all children and mosquitoes within the cluster area. (2) We were unable to characterize the serotype of all DENV infections among village enrollees given restrictions in the frequency of collecting blood from children. (3) We did not collect data on human mobility/behavior that may have influenced the dynamics of transmission within the villages. (4) The possible contribution of adults to DENV transmission was not studied. (5) We did not study the seroprevalence profiles of cluster enrollees. Future studies should focus on positive clusters to more fully characterize the transmission dynamics, the impact of human behavior on transmission patterns, the appropriate spatial scale for disease surveillance/control, and identify more practical and cost-effective approaches to rapid dengue diagnosis. Our cluster methodology provided additional epidemiologic insights. Of note, 14 of the 27 cases of dengue among enrollees were clinically inapparent during this period when DENV-4 was the primary serotype circulating. Most (five of six) primary DENV infections detected in our study were clinically inapparent, similar to observations during a predominantly DENV-2 transmission year in Bangkok [38]. The nearly 1:1 ratio of inapparent to symptomatic secondary DENV infections in our study is also consistent with previous results from KPP [19]. DHF occurred in one (8%) of 12 symptomatic infections and one (4%) of 27 DENV infections confirming that severe dengue represents only a small fraction of the total DENV burden. Future cluster studies can complement these clinical and virologic data by examining correlates of protection that limit transmission, early immunologic events via postinoculation pre-illness specimens and their association with disease severity and sequence variation among viruses through time and space as they circulate between human and mosquito hosts. The prospective cluster methodology utilized here and by others [20] has the potential for broad application. It can be used for multidisciplinary transmission studies of other vector-borne viral diseases as well as spatially and temporally clustered infectious diseases. Supporting Information Figure S1 The Predicted Probability of Infection for Enrollees within Positive Clusters as a Function of Distance to the Index House The probabilities are given for males and females ages 3, 8, and 13 y. Model parameters are reported in Table 5. (51 KB DOC) Click here for additional data file.
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Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru.
Arthur Getis, Amy C Morrison, Kenneth G. Gray … (2003)
We determine the spatial pattern of Aedes aegypti and the containers in which they develop in two neighborhoods of the Amazonian city of Iquitos, Peru. Four variables were examined: adult Ae. aegypti, pupae, containers positive for larvae or pupae, and all water-holding containers. Adults clustered strongly within houses and weakly to a distance of 30 meters beyond the household; clustering was not detected beyond 10 meters for positive containers or pupae. Over short periods of time restricted flight range and frequent blood-feeding behavior of Ae. aegypti appear to be underlying factors in the clustering patterns of human dengue infections. Permanent, consistently infested containers (key premises) were not major producers of Ae. aegypti, indicating that larvaciding strategies by themselves may be less effective than reduction of mosquito development sites by source reduction and education campaigns. We conclude that entomologic risk of human dengue infection should be assessed at the household level at frequent time intervals.
Author and article information
Journal
Journal ID (nlm-ta): Am J Trop Med Hyg
Journal ID (publisher-id): tpmd
Title:
The American Journal of Tropical Medicine and Hygiene
Publisher:
The American Society of Tropical Medicine and Hygiene
ISSN
(Print):
0002-9637
ISSN
(Electronic):
1476-1645
Publication date
(Print):
01
December
2011
Publication date PMC-release: 01
December
2011
Volume: 85
Issue: 6
Pages: 1087-1092
Affiliations
Author notes
*Address correspondence to Roberto Barrera, Entomology and Ecology Activity, Dengue
Branch, Centers for Disease Control and Prevention, Calle Cañada, San Juan, Puerto
Rico 00920. E-mail:
rbarrera@
123456cdc.gov
Article
DOI: 10.4269/ajtmh.2011.11-0381
PMC ID: 3225157
PubMed ID: 22144449
SO-VID: 18d3b4da-da8b-4ec2-8a79-7c3dd0333ac5
Copyright © ©The American Society of Tropical Medicine and Hygiene
License:
This is an Open Access article distributed under the terms of the American Society of Tropical Medicine and Hygiene's Re-use License which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
History
Date
received
: 17
June
2011
Date
accepted
: 16
July
2011
Categories
Subject:
Articles
ScienceOpen disciplines: Infectious disease & Microbiology
Data availability:
ScienceOpen disciplines: Infectious disease & Microbiology