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      Seasonal Dynamics of Phlebotomine Sand Fly Species Proven Vectors of Mediterranean Leishmaniasis Caused by Leishmania infantum

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      1 , 2 , 2 , 2 , 3 , 3 , 3 , 4 , 4 , 4 , 4 , 4 , 4 , 4 , 4 , 5 , 5 , 5 , 6 , 6 , 6 , 7 , 7 , 8 , 8 , 9 , 1 , 1 , 1 , 10 , 11 , 11 , 11 , 5 , 12 , 5 , *
      PLoS Neglected Tropical Diseases
      Public Library of Science

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          Abstract

          Background

          The recent geographical expansion of phlebotomine vectors of Leishmania infantum in the Mediterranean subregion has been attributed to ongoing climate changes. At these latitudes, the activity of sand flies is typically seasonal; because seasonal phenomena are also sensitive to general variations in climate, current phenological data sets can provide a baseline for continuing investigations on sand fly population dynamics that may impact on future scenarios of leishmaniasis transmission. With this aim, in 2011–2013 a consortium of partners from eight Mediterranean countries carried out entomological investigations in sites where L. infantum transmission was recently reported.

          Methods/Principal Findings

          A common protocol for sand fly collection included monthly captures by CDC light traps, complemented by sticky traps in most of the sites. Collections were replicated for more than one season in order to reduce the effects of local weather events. In each site, the trapping effort was left unchanged throughout the survey to legitimate inter-seasonal comparisons. Data from 99,000 collected specimens were analyzed, resulting in the description of seasonal dynamics of 56,000 sand flies belonging to L. infantum vector species throughout a wide geographical area, namely P. perniciosus (Portugal, Spain and Italy), P. ariasi (France), P. neglectus (Greece), P. tobbi (Cyprus and Turkey), P. balcanicus and P. kandelakii (Georgia). Time of sand fly appearance/disappearance in collections differed between sites, and seasonal densities showed variations in each site. Significant correlations were found between latitude/mean annual temperature of sites and i) the first month of sand fly appearance, that ranged from early April to the first half of June; ii) the type of density trend, varying from a single peak in July/August to multiple peaks increasing in magnitude from May through September. A 3-modal trend, recorded for P. tobbi in Cyprus, represents a novel finding for a L. infantum vector. Adults ended the activity starting from mid September through November, without significant correlation with latitude/mean annual temperature of sites. The period of potential exposure to L. infantum in the Mediterranean subregion, as inferred by adult densities calculated from 3 years, 37 sites and 6 competent vector species, was associated to a regular bell-shaped density curve having a wide peak center encompassing the July-September period, and falling between early May to late October for more than 99% of values. Apparently no risk for leishmaniasis transmission took place from December through March in the years considered. We found a common pattern of nocturnal females activity, whose density peaked between 11 pm and 2 am.

          Conclusions

          Despite annual variations, multiple collections performed over consecutive years provided homogeneous patterns of the potential behavior of leishmaniasis vectors in selected sites, which we propose may represent sentinel areas for future monitoring. In the investigated years, higher potential risk for L. infantum transmission in the Mediterranean was identified in the June-October period (97% relative vector density), however such risk was not equally distributed throughout the region, since density waves of adults occurred earlier and were more frequent in southern territories.

          Author Summary

          Recent projections on global warming indicate a constant rise of temperatures in the Mediterranean subregion in the near-mid future. While this phenomenon already caused geographical expansion of several arthropod-borne diseases, it is likely to affect also temporal parameters of seasonally transmitted diseases such as leishmaniasis, a protozoan infection spread by the bite of phlebotomine sand flies. Phenology of sand flies consists in the periods of emergence of adults and their disappearance from collections following an activity period during warm months, which can be characterized by peaks of abundance. Current phenological observations can be important for continuing investigations on sand fly dynamics that may impact on leishmaniasis transmission in the future. With this aim, partners from eight Mediterranean countries identified sites with documented Leishmania infantum transmission by six different vector species and performed multiannual trappings. From the high number of 56,000 specimens collected throughout an area spanning from Portugal at west to Georgia at east, the current seasonal dynamics of Mediterranean vectors was obtained. Both, period of adults emergence and type of density trend were found to be significantly correlated with latitude or mean annual temperature of trapping sites. At the southernmost latitudes, vector activity started as early as begin of April and ended by late November, showing that the no-risk period of potential exposure to L. infantum lasted only 4 months.

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          Most cited references57

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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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            Biology of phlebotomine sand flies as vectors of disease agents.

            Paul Ready (2013)
            Phlebotomines are the sole or principal vectors of Leishmania, Bartonella bacilliformis, and some arboviruses. The coevolution of sand flies with Leishmania species of mammals and lizards is considered in relation to the landscape epidemiology of leishmaniasis, a neglected tropical disease. Evolutionary hypotheses are unresolved, so a practical phlebotomine classification is proposed to aid biomedical information retrieval. The vectors of Leishmania are tabulated and new criteria for their incrimination are given. Research on fly-parasite-host interactions, fly saliva, and behavioral ecology is reviewed in relation to parasite manipulation of blood feeding, vaccine targets, and pheromones for lures. Much basic research is based on few transmission cycles, so generalizations should be made with caution. Integrated research and control programs have begun, but improved control of leishmaniasis and nuisance-biting requires greater emphasis on population genetics and transmission modeling. Most leishmaniasis transmission is zoonotic, affecting the poor and tourists in rural and natural areas, and therefore control should be compatible with environmental conservation.
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              The biology and control of phlebotomine sand flies.

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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
                22 February 2016
                February 2016
                : 10
                : 2
                : e0004458
                Affiliations
                [1 ]Department of Biology, Ecology Division, HUESRL-VERG laboratories, Hacettepe University, Ankara, Turkey
                [2 ]Instituto de Higiene e Medicina Tropical, Unidade Parasitologia Médica, Universidade Nova de Lisboa, Portugal
                [3 ]Centro Nacional de Microbiologia, Servicio de Parasitología, Unidad de Entomología Médica, Instituto de Salud Carlos III, Majadahonda, Madrid, Spain
                [4 ]Institut de Recherche pour le Développement, MIVEGEC, Montpellier, France
                [5 ]M.I.P.I. Department, Unit of Vector-borne Diseases and International Health, Istituto Superiore di Sanità, Rome, Italy
                [6 ]Laboratory of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine, University of Crete, Heraklion, Greece
                [7 ]Veterinary Services of Cyprus, Nicosia, Cyprus
                [8 ]Department of Parasitology, Ege University, Izmir, Turkey
                [9 ]Vocational School of Health Sciences, Cela Bayar University, Manisa, Turkey
                [10 ]Veterinary Faculty, Mehmet Akif Ersoy University, Burdur, Turkey
                [11 ]National Center for Disease Control and Public Health, Tbilisi, Georgia
                [12 ]Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic
                Lancaster University, UNITED KINGDOM
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BA CM LC MJ RM ALB DS MA YO EGo MG PV LG. Performed the experiments: BA CM MOA LC MJ EGo RM ALB JP BV CT CC NR MT DS GB RB CK NTsi ED MA VC AM MK YO SKA OEK FG GO SK NTse LT EGi MG LG. Analyzed the data: BA GB PV LG. Wrote the paper: LG BA PV.

                Article
                PNTD-D-15-00977
                10.1371/journal.pntd.0004458
                4762948
                26900688
                865af4ac-6ecd-4e71-9fde-39a3e56dec0f
                © 2016 Alten 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
                : 9 June 2015
                : 22 January 2016
                Page count
                Figures: 8, Tables: 2, Pages: 22
                Funding
                This study was partially funded by EU grant FP7-261504 EDENext and is catalogued by the EDENext Steering Committee as EDENext376 ( http://www.edenext.eu). The work of CM was done under the fellowship SFRH/BPD/44082/2008 from Fundação para a Ciência e a Tecnologia, Ministério da Educação e Ciência, Portugal. The contents of this publication are the sole responsibility of the authors and do not necessarily reflect the views of the European Commission. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Insect Vectors
                Sand Flies
                Biology and Life Sciences
                Organisms
                Protozoans
                Parasitic Protozoans
                Leishmania
                Leishmania Infantum
                Earth Sciences
                Geography
                Cartography
                Latitude
                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
                Earth Sciences
                Seasons
                People and Places
                Geographical Locations
                Europe
                Portugal
                People and Places
                Geographical Locations
                Asia
                Turkey (Country)
                People and Places
                Geographical Locations
                Europe
                Turkey (Country)
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Diptera
                Phlebotomus
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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