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      Population Dynamics of Aedes aegypti and Dengue as Influenced by Weather and Human Behavior in San Juan, Puerto Rico

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          Abstract

          Previous studies on the influence of weather on Aedes aegypti dynamics in Puerto Rico suggested that rainfall was a significant driver of immature mosquito populations and dengue incidence, but mostly in the drier areas of the island. We conducted a longitudinal study of Ae. aegypti in two neighborhoods of the metropolitan area of San Juan city, Puerto Rico where rainfall is more uniformly distributed throughout the year. We assessed the impacts of rainfall, temperature, and human activities on the temporal dynamics of adult Ae. aegypti and oviposition. Changes in adult mosquitoes were monitored with BG-Sentinel traps and oviposition activity with CDC enhanced ovitraps. Pupal surveys were conducted during the drier and wetter parts of the year in both neighborhoods to determine the contribution of humans and rains to mosquito production. Mosquito dynamics in each neighborhood was compared with dengue incidence in their respective municipalities during the study. Our results showed that: 1. Most pupae were produced in containers managed by people, which explains the prevalence of adult mosquitoes at times when rainfall was scant; 2. Water meters were documented for the first time as productive habitats for Ae. aegypti; 3. Even though Puerto Rico has a reliable supply of tap water and an active tire recycling program, water storage containers and discarded tires were important mosquito producers; 4. Peaks in mosquito density preceded maximum dengue incidence; and 5. Ae. aegypti dynamics were driven by weather and human activity and oviposition was significantly correlated with dengue incidence.

          Author Summary

          Previous studies on the influence of weather on Aedes aegypti in Puerto Rico suggested that rainfall influenced mosquito populations and dengue incidence in the drier areas of the island. We studied temporal changes in Ae. aegypti in areas where rainfall is more uniformly distributed throughout the year. Changes in adult mosquitoes were monitored with BG-Sentinel traps and oviposition activity with CDC enhanced ovitraps. We also counted the number of mosquito pupae in containers with water during the drier and wetter parts of the year to determine the contribution of humans and rainfall to mosquito production. Mosquito dynamics was compared with dengue incidence in the municipalities investigated in the study (November 2007–December 2008). We found that the population of Ae. aegypti was driven by weather and human activities, and peaks in mosquito density preceded maximum dengue incidence during the rainy season. Even though Puerto Rico has a reliable supply of tap water and an active tire recycling program, water storage containers (e.g., 5-gal pails, drums) and discarded tires were important mosquito producers. We also documented for the first time that water meters are important producers of Ae. aegypti. This longitudinal study contributes to a better understanding of the complex dynamics of weather, human behavior, mosquito vectors, and dengue virus transmission in an endemic country.

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          Most cited references76

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          Dengue and dengue haemorrhagic fever.

          The incidence and geographical distribution of dengue have greatly increased in recent years. Dengue is an acute mosquito-transmitted viral disease characterised by fever, headache, muscle and joint pains, rash, nausea, and vomiting. Some infections result in dengue haemorrhagic fever (DHF), a syndrome that in its most severe form can threaten the patient's life, primarily through increased vascular permeability and shock. The case fatality rate in patients with dengue shock syndrome can be as high as 44%. For decades, two distinct hypotheses to explain the mechanism of DHF have been debated-secondary infection or viral virulence. However, a combination of both now seems to be the plausible explanation. The geographical expansion of DHF presents the need for well-documented clinical, epidemiological, and virological descriptions of the syndrome in the Americas. Biological and social research are essential to develop effective mosquito control, medications to reduce capillary leakage, and a safe tetravalent vaccine.
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            Dengue virus-mosquito interactions.

            The mosquito Aedes aegypti is more widely dispersed now than at any time in the past, placing billions of humans at risk of infection with one or more of the four dengue viruses. This review presents and discusses information on mosquito-dengue infection dynamics and describes the prominent role that temperature and rainfall play in controlling dengue viral transmission including discussions of the effect of interannual climate variations and the predicted effect of global warming. Complementary human determinants of dengue epidemiology include viremia titer, variation in viremic period, enhanced viremias, and threshold viremia. Topics covered include epidemiological phenomena such as traveling waves, the generation of genetic diversity of dengue viruses following virgin soil introductions and in hyperendemic settings, and evidence for and against viral virulence as a determinant of the severity of dengue infections. Also described is the crucial role of monotypic and heterotypic herd immunity in shaping dengue epidemic behavior.
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              Ecological and immunological determinants of dengue epidemics.

              The management of infectious diseases is an increasingly important public health issue, the effective implementation of which is often complicated by difficulties in teasing apart the relative roles of extrinsic and intrinsic factors influencing transmission. Dengue, a vector-borne strain polymorphic disease, is one such infection where transmission dynamics are affected by environmental variables as well as immune-mediated serotype interactions. To understand how alternative hypotheses concerning dengue infection and transmission may explain observed multiannual cycles in disease incidence, we adopt a theoretical approach that combines both ecological and immunological mechanisms. We demonstrate that, contrary to perceived wisdom, patterns generated solely by antibody-dependent enhancement or heterogeneity in virus virulence are not consistent with serotype-specific notification data in important ways. Furthermore, to generate epidemics with the characteristic signatures observed in data, we find that a combination of seasonal variation in vector demography and, crucially, a short-lived period of cross-immunity is sufficient. We then show how understanding the persistence and eradication of dengue serotypes critically depends on the alternative assumed mechanisms.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                December 2011
                20 December 2011
                : 5
                : 12
                : e1378
                Affiliations
                [1]Entomology and Ecology Activity, Dengue Branch, Centers for Disease Control and Prevention, Calle Cañada, San Juan, Puerto Rico
                USAMRIID, United States of America
                Author notes

                Conceived and designed the experiments: RB. Performed the experiments: RB MA AJM. Analyzed the data: RB. Contributed reagents/materials/analysis tools: RB MA AJM. Wrote the paper: RB.

                Article
                PNTD-D-11-00395
                10.1371/journal.pntd.0001378
                3243685
                22206021
                6339d24e-bfdf-4549-8e58-5902e1fe3244
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 2 May 2011
                : 13 September 2011
                Page count
                Pages: 9
                Categories
                Research Article
                Biology
                Ecology
                Population Ecology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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