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      A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies

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          Abstract

          Background

          The aim of this study is to describe the major evolutionary historical events among Leishmania, sandflies, and the associated animal reservoirs in detail, in accordance with the geographical evolution of the Earth, which has not been previously discussed on a large scale.

          Methodology and Principal Findings

          Leishmania and sandfly classification has always been a controversial matter, and the increasing number of species currently described further complicates this issue. Despite several hypotheses on the origin, evolution, and distribution of Leishmania and sandflies in the Old and New World, no consistent agreement exists regarding dissemination of the actors that play roles in leishmaniasis. For this purpose, we present here three centuries of research on sandflies and Leishmania descriptions, as well as a complete description of Leishmania and sandfly fossils and the emergence date of each Leishmania and sandfly group during different geographical periods, from 550 million years ago until now. We discuss critically the different approaches that were used for Leishmana and sandfly classification and their synonymies, proposing an updated classification for each species of Leishmania and sandfly. We update information on the current distribution and dispersion of different species of Leishmania (53), sandflies (more than 800 at genus or subgenus level), and animal reservoirs in each of the following geographical ecozones: Palearctic, Nearctic, Neotropic, Afrotropical, Oriental, Malagasy, and Australian. We propose an updated list of the potential and proven sandfly vectors for each Leishmania species in the Old and New World. Finally, we address a classical question about digenetic Leishmania evolution: which was the first host, a vertebrate or an invertebrate?

          Conclusions and Significance

          We propose an updated view of events that have played important roles in the geographical dispersion of sandflies, in relation to both the Leishmania species they transmit and the animal reservoirs of the parasites.

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          Most cited references 251

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          Leishmaniasis Worldwide and Global Estimates of Its Incidence

          As part of a World Health Organization-led effort to update the empirical evidence base for the leishmaniases, national experts provided leishmaniasis case data for the last 5 years and information regarding treatment and control in their respective countries and a comprehensive literature review was conducted covering publications on leishmaniasis in 98 countries and three territories (see ‘Leishmaniasis Country Profiles Text S1, S2, S3, S4, S5, S6, S7, S8, S9, S10, S11, S12, S13, S14, S15, S16, S17, S18, S19, S20, S21, S22, S23, S24, S25, S26, S27, S28, S29, S30, S31, S32, S33, S34, S35, S36, S37, S38, S39, S40, S41, S42, S43, S44, S45, S46, S47, S48, S49, S50, S51, S52, S53, S54, S55, S56, S57, S58, S59, S60, S61, S62, S63, S64, S65, S66, S67, S68, S69, S70, S71, S72, S73, S74, S75, S76, S77, S78, S79, S80, S81, S82, S83, S84, S85, S86, S87, S88, S89, S90, S91, S92, S93, S94, S95, S96, S97, S98, S99, S100, S101’). Additional information was collated during meetings conducted at WHO regional level between 2007 and 2011. Two questionnaires regarding epidemiology and drug access were completed by experts and national program managers. Visceral and cutaneous leishmaniasis incidence ranges were estimated by country and epidemiological region based on reported incidence, underreporting rates if available, and the judgment of national and international experts. Based on these estimates, approximately 0.2 to 0.4 cases and 0.7 to 1.2 million VL and CL cases, respectively, occur each year. More than 90% of global VL cases occur in six countries: India, Bangladesh, Sudan, South Sudan, Ethiopia and Brazil. Cutaneous leishmaniasis is more widely distributed, with about one-third of cases occurring in each of three epidemiological regions, the Americas, the Mediterranean basin, and western Asia from the Middle East to Central Asia. The ten countries with the highest estimated case counts, Afghanistan, Algeria, Colombia, Brazil, Iran, Syria, Ethiopia, North Sudan, Costa Rica and Peru, together account for 70 to 75% of global estimated CL incidence. Mortality data were extremely sparse and generally represent hospital-based deaths only. Using an overall case-fatality rate of 10%, we reach a tentative estimate of 20,000 to 40,000 leishmaniasis deaths per year. Although the information is very poor in a number of countries, this is the first in-depth exercise to better estimate the real impact of leishmaniasis. These data should help to define control strategies and reinforce leishmaniasis advocacy.
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            Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern.

            Phlebotomine sandflies transmit pathogens that affect humans and animals worldwide. We review the roles of phlebotomines in the spreading of leishmaniases, sandfly fever, summer meningitis, vesicular stomatitis, Chandipura virus encephalitis and Carrión's disease. Among over 800 species of sandfly recorded, 98 are proven or suspected vectors of human leishmaniases; these include 42 Phlebotomus species in the Old World and 56 Lutzomyia species in the New World (all: Diptera: Psychodidae). Based on incrimination criteria, we provide an updated list of proven or suspected vector species by endemic country where data are available. Increases in sandfly diffusion and density resulting from increases in breeding sites and blood sources, and the interruption of vector control activities contribute to the spreading of leishmaniasis in the settings of human migration, deforestation, urbanization and conflict. In addition, climatic changes can be expected to affect the density and dispersion of sandflies. Phlebovirus infections and diseases are present in large areas of the Old World, especially in the Mediterranean subregion, in which virus diversity has proven to be higher than initially suspected. Vesiculovirus diseases are important to livestock and humans in the southeastern U.S.A. and Latin America, and represent emerging human threats in parts of India. Carrión's disease, formerly restricted to regions of elevated altitude in Peru, Ecuador and Colombia, has shown recent expansion to non-endemic areas of the Amazon basin. © 2012 The Authors. Medical and Veterinary Entomology © 2012 The Royal Entomological Society.
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              Phylogenetic Systematics

               Willi Hennig (1965)
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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, CA USA )
                1935-2727
                1935-2735
                3 March 2016
                March 2016
                : 10
                : 3
                Affiliations
                [1 ]Service de Parasitologie-Mycologie, Hôpital de l’Archet, Centre Hospitalier Universitaire de Nice, Nice, France
                [2 ]Division of Molecular Biotechnology and Functional Genetics, Technical University of Applied Sciences Wildau, Wildau, Germany
                [3 ]Inserm U1065, Centre Méditerranéen de Médecine Moléculaire, Université de Nice-Sophia Antipolis, Nice, France
                [4 ]Biology Centre, Institute of Parasitology, Czech Academy of Sciences, Prague, Czech Republic
                [5 ]Department of Parasitology, Faculty of Science, Charles University in Prague, Prague, Czech Republic
                [6 ]MIVEGEC, UMR CNRS-IRD-Université de Montpellier Centre IRD, Montpellier, France
                [7 ]UMR177, Centre IRD de Montpellier, Montpellier, France
                Institut de Recherche pour le Développement, FRANCE
                Author notes

                The authors have declared that no competing interests exist.

                Article
                PNTD-D-15-01274
                10.1371/journal.pntd.0004349
                4777430
                26937644
                © 2016 Akhoundi 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.

                Page count
                Figures: 3, Tables: 4, Pages: 40
                Product
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Review
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Leishmania
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Insect Vectors
                Sand Flies
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Diptera
                Phlebotomus
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                Biology and Life Sciences
                Parasitology
                Parasite Evolution
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Mammals
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogenesis
                Host-Pathogen Interactions
                Biology and Life Sciences
                Paleontology
                Paleobiology
                Paleozoology
                Earth Sciences
                Paleontology
                Paleobiology
                Paleozoology

                Infectious disease & Microbiology

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