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      A Non-Stationary Relationship between Global Climate Phenomena and Human Plague Incidence in Madagascar

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          Abstract

          Background

          Plague, a zoonosis caused by Yersinia pestis, is found in Asia and the Americas, but predominantly in Africa, with the island of Madagascar reporting almost one third of human cases worldwide. Plague's occurrence is affected by local climate factors which in turn are influenced by large-scale climate phenomena such as the El Niño Southern Oscillation (ENSO). The effects of ENSO on regional climate are often enhanced or reduced by a second large-scale climate phenomenon, the Indian Ocean Dipole (IOD). It is known that ENSO and the IOD interact as drivers of disease. Yet the impacts of these phenomena in driving plague dynamics via their effect on regional climate, and specifically contributing to the foci of transmission on Madagascar, are unknown. Here we present the first analysis of the effects of ENSO and IOD on plague in Madagascar.

          Methodology/principal findings

          We use a forty-eight year monthly time-series of reported human plague cases from 1960 to 2008. Using wavelet analysis, we show that over the last fifty years there have been complex non-stationary associations between ENSO/IOD and the dynamics of plague in Madagascar. We demonstrate that ENSO and IOD influence temperature in Madagascar and that temperature and plague cycles are associated. The effects on plague appear to be mediated more by temperature, but precipitation also undoubtedly influences plague in Madagascar. Our results confirm a relationship between plague anomalies and an increase in the intensity of ENSO events and precipitation.

          Conclusions/significance

          This work widens the understanding of how climate factors acting over different temporal scales can combine to drive local disease dynamics. Given the association of increasing ENSO strength and plague anomalies in Madagascar it may in future be possible to forecast plague outbreaks in Madagascar. The study gives insight into the complex and changing relationship between climate factors and plague in Madagascar.

          Author Summary

          Plague is a vector-borne bacterial infection with rodents and their fleas as its principal hosts. Transmission to humans occurs via the bite of an infected flea. In the highlands of Madagascar, plague is endemic and more than one hundred human cases are reported every year. Global climate is known to affect many infectious diseases and has been shown to affect plague incidence in other areas of the world. The ENSO and the IOD are global climate drivers affecting rainfall and temperature in Madagascar. Our study investigates the effect of global climate drivers on human plague incidence on the island. We found a link between ENSO, IOD, temperature and precipitation and plague incidence throughout the 48-year time-series although it was not constant over time. The correlation between ENSO and plague turned from weakly positive to strongly negative and then to positive, and the association with the IOD became stronger with time. We demonstrate that during periods of high ENSO intensity, plague incidence is likely to increase via ENSO's impact on temperature and precipitation. This shows that climate indices can be a tool to help predict human plague incidence.

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          Most cited references22

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          Impact of regional climate change on human health.

          The World Health Organisation estimates that the warming and precipitation trends due to anthropogenic climate change of the past 30 years already claim over 150,000 lives annually. Many prevalent human diseases are linked to climate fluctuations, from cardiovascular mortality and respiratory illnesses due to heatwaves, to altered transmission of infectious diseases and malnutrition from crop failures. Uncertainty remains in attributing the expansion or resurgence of diseases to climate change, owing to lack of long-term, high-quality data sets as well as the large influence of socio-economic factors and changes in immunity and drug resistance. Here we review the growing evidence that climate-health relationships pose increasing health risks under future projections of climate change and that the warming trend over recent decades has already contributed to increased morbidity and mortality in many regions of the world. Potentially vulnerable regions include the temperate latitudes, which are projected to warm disproportionately, the regions around the Pacific and Indian oceans that are currently subjected to large rainfall variability due to the El Niño/Southern Oscillation sub-Saharan Africa and sprawling cities where the urban heat island effect could intensify extreme climatic events.
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            Wavelet analysis of ecological time series.

            Wavelet analysis is a powerful tool that is already in use throughout science and engineering. The versatility and attractiveness of the wavelet approach lie in its decomposition properties, principally its time-scale localization. It is especially relevant to the analysis of non-stationary systems, i.e., systems with short-lived transient components, like those observed in ecological systems. Here, we review the basic properties of the wavelet approach for time-series analysis from an ecological perspective. Wavelet decomposition offers several advantages that are discussed in this paper and illustrated by appropriate synthetic and ecological examples. Wavelet analysis is notably free from the assumption of stationarity that makes most methods unsuitable for many ecological time series. Wavelet analysis also permits analysis of the relationships between two signals, and it is especially appropriate for following gradual change in forcing by exogenous variables.
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              Climate and vectorborne diseases.

              Climate change could significantly affect vectorborne disease in humans. Temperature, precipitation, humidity, and other climatic factors are known to affect the reproduction, development, behavior, and population dynamics of the arthropod vectors of these diseases. Climate also can affect the development of pathogens in vectors, as well as the population dynamics and ranges of the nonhuman vertebrate reservoirs of many vectorborne diseases. Whether climate changes increase or decrease the incidence of vectorborne diseases in humans will depend not only on the actual climatic conditions but also on local nonclimatic epidemiologic and ecologic factors. Predicting the relative impact of sustained climate change on vectorborne diseases is difficult and will require long-term studies that look not only at the effects of climate change but also at the contributions of other agents of global change such as increased trade and travel, demographic shifts, civil unrest, changes in land use, water availability, and other issues. Adapting to the effects of climate change will require the development of adequate response plans, enhancement of surveillance systems, and development of effective and locally appropriate strategies to control and prevent vectorborne diseases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                October 2014
                9 October 2014
                : 8
                : 10
                : e3155
                Affiliations
                [1 ]LUCINDA group, Institute of Infection and Global Health, Department of Epidemiology and Population Health, University of Liverpool, Neston, United Kingdom
                [2 ]Department of Geography and Planning, School of Environmental Sciences, University of Liverpool, Liverpool, Merseyside, United Kingdom
                [3 ]Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom
                [4 ]Unité Peste - Institut Pasteur de Madagascar, Antananarivo, Madagascar
                [5 ]Centers for Disease Control and Prevention, Division of Bacterial Diseases, Atlanta, Georgia, United States of America
                [6 ]Health Protection Research Unit in Emerging and Zoonotic Infections, University of Liverpool, Neston, United Kingdom
                Yale University, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CC KSK MB AM ST. Analyzed the data: KSK CC MB. Wrote the paper: KSK MB CC ST. Compilation of data: MR LR.

                Article
                PNTD-D-13-00728
                10.1371/journal.pntd.0003155
                4191945
                25299064
                c45e67bb-e402-4b5d-8111-27555218a332
                Copyright @ 2014

                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
                : 23 May 2013
                : 31 July 2014
                Page count
                Pages: 13
                Funding
                The analysis of the study was supported by the Leverhulme Trust Research Leadership Award F/0025/AC: “Predicting the effects of climate change on infectious diseases of animals” (awarded to MB). Funding for KSK was provided by a University of Liverpool PhD studentship award and for MB by BBSRC award ISIS 1813, “Climate change and the future of plague in Madagascar.” The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Yersinia
                Yersinia Pestis
                Plant Science
                Plant Pathology
                Infectious Disease Epidemiology
                Earth Sciences
                Ecology and Environmental Sciences
                Medicine and Health Sciences
                Epidemiology
                Infectious Diseases
                Bacterial Diseases
                Public and Occupational Health
                Global Health
                Tropical Diseases
                Neglected Tropical Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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