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      Modeling the epidemiological history of plague in Central Asia: Palaeoclimatic forcing on a disease system over the past millennium

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          Abstract

          Background

          Human cases of plague ( Yersinia pestis) infection originate, ultimately, in the bacterium's wildlife host populations. The epidemiological dynamics of the wildlife reservoir therefore determine the abundance, distribution and evolution of the pathogen, which in turn shape the frequency, distribution and virulence of human cases. Earlier studies have shown clear evidence of climatic forcing on contemporary plague abundance in rodents and humans.

          Results

          We find that high-resolution palaeoclimatic indices correlate with plague prevalence and population density in a major plague host species, the great gerbil ( Rhombomys opimus), over 1949-1995. Climate-driven models trained on these data predict independent data on human plague cases in early 20th-century Kazakhstan from 1904-1948, suggesting a consistent impact of climate on large-scale wildlife reservoir dynamics influencing human epidemics. Extending the models further back in time, we also find correspondence between their predictions and qualitative records of plague epidemics over the past 1500 years.

          Conclusions

          Central Asian climate fluctuations appear to have had significant influences on regional human plague frequency in the first part of the 20th century, and probably over the past 1500 years. This first attempt at ecoepidemiological reconstruction of historical disease activity may shed some light on how long-term plague epidemiology interacts with human activity. As plague activity in Central Asia seems to have followed climate fluctuations over the past centuries, we may expect global warming to have an impact upon future plague epidemiology, probably sustaining or increasing plague activity in the region, at least in the rodent reservoirs, in the coming decades.

          See commentary: http://www.biomedcentral.com/1741-7007/8/108

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          Most cited references41

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          Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis.

          Plague, one of the most devastating diseases of human history, is caused by Yersinia pestis. In this study, we analyzed the population genetic structure of Y. pestis and the two other pathogenic Yersinia species, Y. pseudotuberculosis and Y. enterocolitica. Fragments of five housekeeping genes and a gene involved in the synthesis of lipopolysaccharide were sequenced from 36 strains representing the global diversity of Y. pestis and from 12-13 strains from each of the other species. No sequence diversity was found in any Y. pestis gene, and these alleles were identical or nearly identical to alleles from Y. pseudotuberculosis. Thus, Y. pestis is a clone that evolved from Y. pseudotuberculosis 1,500-20,000 years ago, shortly before the first known pandemics of human plague. Three biovars (Antiqua, Medievalis, and Orientalis) have been distinguished by microbiologists within the Y. pestis clone. These biovars form distinct branches of a phylogenetic tree based on restriction fragment length polymorphisms of the locations of the IS100 insertion element. These data are consistent with previous inferences that Antiqua caused a plague pandemic in the sixth century, Medievalis caused the Black Death and subsequent epidemics during the second pandemic wave, and Orientalis caused the current plague pandemic.
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            Plague: Past, Present, and Future

            The authors argue that plague should be taken much more seriously by the international health community.
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              Microevolution and history of the plague bacillus, Yersinia pestis.

              The association of historical plague pandemics with Yersinia pestis remains controversial, partly because the evolutionary history of this largely monomorphic bacterium was unknown. The microevolution of Y. pestis was therefore investigated by three different multilocus molecular methods, targeting genomewide synonymous SNPs, variation in number of tandem repeats, and insertion of IS100 insertion elements. Eight populations were recognized by the three methods, and we propose an evolutionary tree for these populations, rooted on Yersinia pseudotuberculosis. The tree invokes microevolution over millennia, during which enzootic pestoides isolates evolved. This initial phase was followed by a binary split 6,500 years ago, which led to populations that are more frequently associated with human disease. These populations do not correspond directly to classical biovars that are based on phenotypic properties. Thus, we recommend that henceforth groupings should be based on molecular signatures. The age of Y. pestis inferred here is compatible with the dates of historical pandemic plague. However, it is premature to infer an association between any modern molecular grouping and a particular pandemic wave that occurred before the 20th century.
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                Author and article information

                Journal
                BMC Biol
                BMC Biology
                BioMed Central
                1741-7007
                2010
                27 August 2010
                : 8
                : 112
                Affiliations
                [1 ]Centre for Ecological and Evolutionary Synthesis (CEES), Dept. of Biology, University of Oslo, P.O. Box 1066, N-0316 Oslo, Norway
                [2 ]School of Biological Sciences, University of Liverpool, Liverpool L69 7ZB, UK
                [3 ]Department of Geography, Johannes Gutenberg University Mainz, 55099 Mainz, Germany
                [4 ]Dendro Sciences Unit, Swiss Federal Research Institute WSL, Switzerland
                [5 ]Dept. of Biology, University of Antwerp, Groenenborgerlaan 171 B-2020, Antwerp, Belgium
                [6 ]Danish Pest Infestation Laboratory, University of Aarhus, Dept. of Integrated Pest Management, Skovbrynet 14, DK-2800 Kongens Lyngby, Denmark
                [7 ]Key Laboratory of Desert and Desertification, Cold and Arid Regions, Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou, 730000, Gansu Province, China
                [8 ]State Key Laboratory of Cryspheric Sciences, Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou 730000, China
                [9 ]State Key Laboratory of Integrated Management on Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
                Article
                1741-7007-8-112
                10.1186/1741-7007-8-112
                2944127
                20799946
                4bb23795-a1e0-49a3-b359-4d2c2ed2d853
                Copyright ©2010 Kausrud et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 April 2010
                : 27 August 2010
                Categories
                Research Article

                Life sciences
                Life sciences

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