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      Climate Change and Risk of Leishmaniasis in North America: Predictions from Ecological Niche Models of Vector and Reservoir Species

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          Abstract

          Background

          Climate change is increasingly being implicated in species' range shifts throughout the world, including those of important vector and reservoir species for infectious diseases. In North America (México, United States, and Canada), leishmaniasis is a vector-borne disease that is autochthonous in México and Texas and has begun to expand its range northward. Further expansion to the north may be facilitated by climate change as more habitat becomes suitable for vector and reservoir species for leishmaniasis.

          Methods and Findings

          The analysis began with the construction of ecological niche models using a maximum entropy algorithm for the distribution of two sand fly vector species ( Lutzomyia anthophora and L. diabolica), three confirmed rodent reservoir species ( Neotoma albigula, N. floridana, and N. micropus), and one potential rodent reservoir species ( N. mexicana) for leishmaniasis in northern México and the United States. As input, these models used species' occurrence records with topographic and climatic parameters as explanatory variables. Models were tested for their ability to predict correctly both a specified fraction of occurrence points set aside for this purpose and occurrence points from an independently derived data set. These models were refined to obtain predicted species' geographical distributions under increasingly strict assumptions about the ability of a species to disperse to suitable habitat and to persist in it, as modulated by its ecological suitability. Models successful at predictions were fitted to the extreme A2 and relatively conservative B2 projected climate scenarios for 2020, 2050, and 2080 using publicly available interpolated climate data from the Third Intergovernmental Panel on Climate Change Assessment Report. Further analyses included estimation of the projected human population that could potentially be exposed to leishmaniasis in 2020, 2050, and 2080 under the A2 and B2 scenarios. All confirmed vector and reservoir species will see an expansion of their potential range towards the north. Thus, leishmaniasis has the potential to expand northwards from México and the southern United States. In the eastern United States its spread is predicted to be limited by the range of L. diabolica; further west, L. anthophora may play the same role. In the east it may even reach the southern boundary of Canada. The risk of spread is greater for the A2 scenario than for the B2 scenario. Even in the latter case, with restrictive (contiguous) models for dispersal of vector and reservoir species, and limiting vector and reservoir species occupancy to only the top 10% of their potential suitable habitat, the expected number of human individuals exposed to leishmaniasis by 2080 will at least double its present value.

          Conclusions

          These models predict that climate change will exacerbate the ecological risk of human exposure to leishmaniasis in areas outside its present range in the United States and, possibly, in parts of southern Canada. This prediction suggests the adoption of measures such as surveillance for leishmaniasis north of Texas as disease cases spread northwards. Potential vector and reservoir control strategies—besides direct intervention in disease cases—should also be further investigated.

          Author Summary

          We explored the consequences of climate change for the spread of leishmaniasis in North America. We modeled the distribution of two sand fly vector and four rodent reservoir species found in northern México and the southern United States. Models were based on occurrence data and environmental and topographic layers. Successful models were projected to 2020, 2050, and 2080 using an extreme (A2) and a conservative (B2) future climate scenario. We predicted potential range shifts of vector and reservoir species varying assumptions about dispersal ability and capacity to persist in habitats with different degrees of ecological suitability. Even with the most conservative assumptions the distributions of both vector and reservoir species expand northwards, potentially reaching as far as southern Canada in the east. Assuming that at least one vector and one reservoir species must be present for a parasite cycle, the extent of this shift is predicted to be controlled by the availability of suitable habitat for sand fly vector species. Finally, we computed the human population potentially exposed to leishmaniasis because of these range shifts. Even in the most optimistic scenario we found that twice as many individuals could be exposed to leishmaniasis in North America in 2080 compared to today.

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          Most cited references32

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          The leishmaniases as emerging and reemerging zoonoses.

          The 20 or so species of Leishmania which have been recorded as human infections are all either zoonotic, or have recent zoonotic origins. Their distribution is determined by that of their vector, their reservoir host, or both, so is dependent on precise environmental features. This concatenation of limiting factors leads to specific environmental requirements and focal distribution of zoonotic or anthroponotic sources. Human infection is dependent on the ecological relationship between human activity and reservoir systems. Examples are available of the emergence of leishmaniasis from the distant past to the present, and can be postulated for the future. These emergences have been provoked by the adoption of new, secondary reservoir hosts, the adoption of new vector species, transport of infection in humans or domestic animals, invasion by humans of zoonotic foci, and irruption of reservoir hosts beyond their normal range. The leishmaniases therefore present an excellent model for emerging disease in general, and for the generation of the principles governing emergence. The model is, however, limited by gaps in our knowledge, usually quantitative, sometimes qualitative, of the structure of reservoir systems.
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            The current status of zoonotic leishmaniases and approaches to disease control.

            Leishmaniases are a complex of world-wide diseases with a range of clinical and epidemiological features caused by Leishmania spp. of protozoan parasites. Among 15 well-recognised Leishmania species known to infect humans, 13 have zoonotic nature, which include agents of visceral, cutaneous and mucocutaneous forms of the disease in both the Old and New Worlds. Currently, leishmaniases show a wider geographic distribution and increased global incidence of human disease than previously known. Environmental, demographic and human behavioural factors contribute to the changing landscape of leishmaniasis, which includes increasing risk factors for zoonotic cutaneous leishmaniases and new scenarios associated with the zoonotic visceral leishmaniases. The latter consist of the northward spread of Leishmania infantum transmission in Europe and America, the identification of unusual mammal hosts, and the decline of HIV-Leishmania co-infections in southern Europe following the introduction of the highly active antiretroviral therapy. Few advances have been made in the surveillance and control of the zoonotic leishmaniasis, however a number of tools have been developed for the control of the canine reservoir of L. infantum. These include: (i) several canine vaccine candidates, in particular an FML Leishmania enriched fraction showing good clinical protection, has been registered in Brazil for veterinary use; (ii) a number of insecticide-based preparations have been specifically registered for dog protection against sand fly bites. Laboratory and field studies have shown improved efficacy of these preparations for both individual and mass protection.
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              Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans.

              Leishmaniases remain a major public health problem today despite the vast amount of research conducted on Leishmania pathogens. The biological model is genetically and ecologically complex. This paper explores the advances in Leishmania genetics and reviews population structure, taxonomy, epidemiology and pathogenicity. Current knowledge of Leishmania genetics is placed in the context of natural populations. Various studies have described a clonal structure for Leishmania but recombination, pseudo-recombination and other genetic processes have also been reported. The impact of these different models on epidemiology and the medical aspects of leishmaniases is considered from an evolutionary point of view. The role of these parasites in the expression of pathogenicity in humans is also explored. It is important to ascertain whether genetic variability of the parasites is related to the different clinical expressions of leishmaniasis. The review aims to put current knowledge of Leishmania and the leishmaniases in perspective and to underline priority questions which 'leishmaniacs' must answer in various domains: epidemiology, population genetics, taxonomy and pathogenicity. It concludes by presenting a number of feasible ways of responding to these questions.
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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 2010
                19 January 2010
                : 4
                : 1
                : e585
                Affiliations
                [1 ]Laboratorio de Sistemas de Información Geográfica, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Coyoacán, México
                [2 ]Department of Geography and the Environment, University of Texas at Austin, Austin, Texas, United States of America
                [3 ]Biodiversity and Biocultural Conservation Laboratory, Section of Integrative Biology, University of Texas at Austin, Austin, Texas, United States of America
                [4 ]Laboratorio de Análisis Especiales, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Coyoacán, México
                Yale University, United States of America
                Author notes

                Conceived and designed the experiments: SS. Analyzed the data: CG OW SES VSC SS. Wrote the paper: CG VSC SS. Built computer models. Built computer models: CGS.

                Article
                09-PNTD-RA-0156R3
                10.1371/journal.pntd.0000585
                2799657
                20098495
                a8e9dd80-ea14-44c1-8797-6f8f41a0d2fb
                González et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 13 April 2009
                : 2 December 2009
                Page count
                Pages: 16
                Categories
                Research Article
                Computational Biology
                Ecology/Global Change Ecology
                Infectious Diseases/Neglected Tropical Diseases
                Public Health and Epidemiology
                Public Health and Epidemiology/Global Health
                Public Health and Epidemiology/Infectious Diseases

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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