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      Climate Teleconnections and Recent Patterns of Human and Animal Disease Outbreaks

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          Abstract

          Background

          Recent clusters of outbreaks of mosquito-borne diseases (Rift Valley fever and chikungunya) in Africa and parts of the Indian Ocean islands illustrate how interannual climate variability influences the changing risk patterns of disease outbreaks. Although Rift Valley fever outbreaks have been known to follow periods of above-normal rainfall, the timing of the outbreak events has largely been unknown. Similarly, there is inadequate knowledge on climate drivers of chikungunya outbreaks. We analyze a variety of climate and satellite-derived vegetation measurements to explain the coupling between patterns of climate variability and disease outbreaks of Rift Valley fever and chikungunya.

          Methods and Findings

          We derived a teleconnections map by correlating long-term monthly global precipitation data with the NINO3.4 sea surface temperature (SST) anomaly index. This map identifies regional hot-spots where rainfall variability may have an influence on the ecology of vector borne disease. Among the regions are Eastern and Southern Africa where outbreaks of chikungunya and Rift Valley fever occurred 2004–2009. Chikungunya and Rift Valley fever case locations were mapped to corresponding climate data anomalies to understand associations between specific anomaly patterns in ecological and climate variables and disease outbreak patterns through space and time. From these maps we explored associations among Rift Valley fever disease occurrence locations and cumulative rainfall and vegetation index anomalies. We illustrated the time lag between the driving climate conditions and the timing of the first case of Rift Valley fever. Results showed that reported outbreaks of Rift Valley fever occurred after ∼3–4 months of sustained above-normal rainfall and associated green-up in vegetation, conditions ideal for Rift Valley fever mosquito vectors. For chikungunya we explored associations among surface air temperature, precipitation anomalies, and chikungunya outbreak locations. We found that chikungunya outbreaks occurred under conditions of anomalously high temperatures and drought over Eastern Africa. However, in Southeast Asia, chikungunya outbreaks were negatively correlated ( p<0.05) with drought conditions, but positively correlated with warmer-than-normal temperatures and rainfall.

          Conclusions/Significance

          Extremes in climate conditions forced by the El Niño/Southern Oscillation (ENSO) lead to severe droughts or floods, ideal ecological conditions for disease vectors to emerge, and may result in epizootics and epidemics of Rift Valley fever and chikungunya. However, the immune status of livestock (Rift Valley fever) and human (chikungunya) populations is a factor that is largely unknown but very likely plays a role in the spatial-temporal patterns of these disease outbreaks. As the frequency and severity of extremes in climate increase, the potential for globalization of vectors and disease is likely to accelerate. Understanding the underlying patterns of global and regional climate variability and their impacts on ecological drivers of vector-borne diseases is critical in long-range planning of appropriate disease and disease-vector response, control, and mitigation strategies.

          Author Summary

          Interannual climate variability associated with the El Niño/Southern Oscillation (ENSO) phenomenon and regional climatic circulation mechanisms in the equatorial Indian Ocean result in significant rainfall and ecological anomaly patterns that are major drivers of spatial and temporal patterns of mosquito-borne disease outbreaks. Correlation and regression analyses of long time series rainfall, vegetation index, and temperature data show that large scale anomalies occur periodically that may influence mosquito vector populations and thus spatial and temporal patterns of Rift Valley fever and chikungunya outbreaks. Rift Valley fever outbreak events occurred after a period of ∼3–4 months of persistent and above-normal rainfall that enabled vector habitats to flourish. On the other hand, chikungunya outbreaks occurred during periods of high temperatures and severe drought over East Africa and the western Indian Ocean islands. This is consistent with highly populated environmental settings where domestic and peri-domestic stored water containers were the likely mosquito sources. However, in Southeast Asia, approximately 52% of chikungunya outbreaks occurred during cooler-than-normal temperatures and were significantly negatively correlated with drought. Besides climate variability, other factors not accounted for such as vertebrate host immunity may contribute to spatio-temporal patterns of outbreaks.

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          Most cited references56

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          Effects of environmental change on emerging parasitic diseases.

          Ecological disturbances exert an influence on the emergence and proliferation of malaria and zoonotic parasitic diseases, including, Leishmaniasis, cryptosporidiosis, giardiasis, trypanosomiasis, schistosomiasis, filariasis, onchocerciasis, and loiasis. Each environmental change, whether occurring as a natural phenomenon or through human intervention, changes the ecological balance and context within which disease hosts or vectors and parasites breed, develop, and transmit disease. Each species occupies a particular ecological niche and vector species sub-populations are distinct behaviourally and genetically as they adapt to man-made environments. Most zoonotic parasites display three distinct life cycles: sylvatic, zoonotic, and anthroponotic. In adapting to changed environmental conditions, including reduced non-human population and increased human population, some vectors display conversion from a primarily zoophyllic to primarily anthrophyllic orientation. Deforestation and ensuing changes in landuse, human settlement, commercial development, road construction, water control systems (dams, canals, irrigation systems, reservoirs), and climate, singly, and in combination have been accompanied by global increases in morbidity and mortality from emergent parasitic disease. The replacement of forests with crop farming, ranching, and raising small animals can create supportive habitats for parasites and their host vectors. When the land use of deforested areas changes, the pattern of human settlement is altered and habitat fragmentation may provide opportunities for exchange and transmission of parasites to the heretofore uninfected humans. Construction of water control projects can lead to shifts in such vector populations as snails and mosquitoes and their parasites. Construction of roads in previously inaccessible forested areas can lead to erosion, and stagnant ponds by blocking the flow of streams when the water rises during the rainy season. The combined effects of environmentally detrimental changes in local land use and alterations in global climate disrupt the natural ecosystem and can increase the risk of transmission of parasitic diseases to the human population.
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            Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus.

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              Two Chikungunya Isolates from the Outbreak of La Reunion (Indian Ocean) Exhibit Different Patterns of Infection in the Mosquito, Aedes albopictus

              Background A Chikungunya (CHIK) outbreak hit La Réunion Island in 2005–2006. The implicated vector was Aedes albopictus. Here, we present the first study on the susceptibility of Ae. albopictus populations to sympatric CHIKV isolates from La Réunion Island and compare it to other virus/vector combinations. Methodology and Findings We orally infected 8 Ae. albopictus collections from La Réunion and 3 from Mayotte collected in March 2006 with two Chikungunya virus (CHIKV) from La Réunion: (i) strain 05.115 collected in June 2005 with an Alanine at the position 226 of the glycoprotein E1 and (ii) strain 06.21 collected in November 2005 with a substitution A226V. Two other CHIKV isolates and four additional mosquito strains/species were also tested. The viral titer of the infectious blood-meal was 107 plaque forming units (pfu)/mL. Dissemination rates were assessed by immunofluorescent staining on head squashes of surviving females 14 days after infection. Rates were at least two times higher with CHIKV 06.21 compared to CHIKV 05.115. In addition, 10 individuals were analyzed every day by quantitative RT-PCR. Viral RNA was quantified on (i) whole females and (ii) midguts and salivary glands of infected females. When comparing profiles, CHIKV 06.21 produced nearly 2 log more viral RNA copies than CHIKV 05.115. Furthermore, females infected with CHIKV 05.115 could be divided in two categories: weakly susceptible or strongly susceptible, comparable to those infected by CHIKV 06.21. Histological analysis detected the presence of CHIKV in salivary glands two days after infection. In addition, Ae. albopictus from La Réunion was as efficient vector as Ae. aegypti and Ae. albopictus from Vietnam when infected with the CHIKV 06.21. Conclusions Our findings support the hypothesis that the CHIK outbreak in La Réunion Island was due to a highly competent vector Ae. albopictus which allowed an efficient replication and dissemination of CHIKV 06.21.
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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
                January 2012
                24 January 2012
                : 6
                : 1
                : e1465
                Affiliations
                [1 ]Biospheric Sciences Laboratory, NASA Goddard Space Flight Center, Greenbelt, Maryland, United States of America
                [2 ]USDA-ARS Center for Medical, Agricultural, & Veterinary Entomology, Gainesville, Florida, United States of America
                [3 ]Clark Labs, Clark University, Worcester, Massachusetts, United States of America
                [4 ]Division of GEIS Operations, Armed Forces Health Surveillance Center, Silver Spring, Maryland, United States of America
                National Institute of Parasitic Diseases China CDC, China
                Author notes

                Conceived and designed the experiments: AA KJL. Performed the experiments: AA KJL JLS KMC EWP. Analyzed the data: AA KJL JLS KMC EWP. Contributed reagents/materials/analysis tools: AA JLS KMC KJL CJT JRE JEP KLR. Wrote the paper: AA KJL JLS KMC CJT SCB JRE JEP KLR. Contributed to data processing and graphic design: EWP JLS KMC AA.

                Article
                PNTD-D-11-00034
                10.1371/journal.pntd.0001465
                3265456
                22292093
                9874e4fe-dd7b-43b3-8a16-6daa31afe300
                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
                : 13 January 2011
                : 21 November 2011
                Page count
                Pages: 14
                Categories
                Research Article
                Biology
                Plant Science
                Ecology
                Population Biology
                Zoology
                Computer Science
                Geoinformatics
                Earth Sciences
                Atmospheric Science
                Atmospheric Dynamics
                Climatology
                Environmental Sciences
                Geography
                Physical Geography
                Veterinary Science
                Veterinary Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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