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      Recent advances in phlebotomine sand fly research related to leishmaniasis control

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          Abstract

          Phlebotomine sand flies are the subject of much research because of the role of their females as the only proven natural vectors of Leishmania species, the parasitic protozoans that are the causative agents of the neglected tropical disease leishmaniasis. Activity in this field was highlighted by the eighth International Symposium on Phlebotomine Sand flies (ISOPS) held in September 2014, which prompted this review focusing on vector control. Topics reviewed include: Taxonomy and phylogenetics, Vector competence, Genetics, genomics and transcriptomics, Eco-epidemiology, and Vector control. Research on sand flies as leishmaniasis vectors has revealed a diverse array of zoonotic and anthroponotic transmission cycles, mostly in subtropical and tropical regions of Africa, Asia and Latin America, but also in Mediterranean Europe. The challenge is to progress beyond descriptive eco-epidemiology, in order to separate vectors of biomedical importance from the sand fly species that are competent vectors but lack the vectorial capacity to cause much human disease. Transmission modelling is required to identify the vectors that are a public health priority, the ones that must be controlled as part of the integrated control of leishmaniasis. Effective modelling of transmission will require the use of entomological indices more precise than those usually reported in the leishmaniasis literature.

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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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            Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies

            A thorough understanding of the transmission mechanism of any infectious agent is crucial to implementing an effective intervention strategy. Here, our current understanding of the mechanisms that Leishmania parasites use to ensure their transmission from sand fly vectors by bite is reviewed. The most important mechanism is the creation of a “blocked fly” resulting from the secretion of promastigote secretory gel (PSG) by the parasites in the anterior midgut. This forces the sand fly to regurgitate PSG before it can bloodfeed, thereby depositing both PSG and infective metacyclic promastigotes in the skin of a mammalian host. Other possible factors in transmission are considered: damage to the stomodeal valve; occurrence of parasites in the salivary glands; and excretion of parasites from the anus of infected sand flies. Differences in the transmission mechanisms employed by parasites in the three subgenera, Leishmania, Viannia and Sauroleishmania are also addressed.
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              Transmission, reservoir hosts and control of zoonotic visceral leishmaniasis.

              Zoonotic visceral leishmaniasis (ZVL) caused by Leishmania infantum is an important disease of humans and dogs. Here we review aspects of the transmission and control of ZVL. Whilst there is clear evidence that ZVL is maintained by sandfly transmission, transmission may also occur by non-sandfly routes, such as congenital and sexual transmission. Dogs are the only confirmed primary reservoir of infection. Meta-analysis of dog studies confirms that infectiousness is higher in symptomatic infection; infectiousness is also higher in European than South American studies. A high prevalence of infection has been reported from an increasing number of domestic and wild mammals; updated host ranges are provided. The crab-eating fox Cerdocyon thous, opossums Didelphis spp., domestic cat Felis cattus, black rat Rattus rattus and humans can infect sandflies, but confirmation of these hosts as primary or secondary reservoirs requires further xenodiagnosis studies at the population level. Thus the putative sylvatic reservoir(s) of ZVL remains unknown. Review of intervention studies examining the effectiveness of current control methods highlights the lack of randomized controlled trials of both dog culling and residual insecticide spraying. Topical insecticides (deltamethrin-impregnated collars and pour-ons) have been shown to provide a high level of individual protection to treated dogs, but further community-level studies are needed.
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                Author and article information

                Contributors
                p.bates@lancaster.ac.uk
                jerome.depaquit@univ-reims.fr
                egalati@usp.br
                skamhawi@niaid.nih.gov
                michele.maroli@gmail.com
                mcdowell.11@nd.edu
                albert.picado@cresib.cat
                Paul.Ready@lshtm.ac.uk
                odanielsalomon@gmail.com
                jayusp@hotmail.com
                ytraub@ioc.fiocruz.br
                alonw@ekmd.huji.ac.il
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                27 February 2015
                27 February 2015
                2015
                : 8
                : 131
                Affiliations
                [ ]Division of Biomedical and Life Sciences, Faculty of Health and Medicine, Lancaster University, Lancaster, UK
                [ ]Université de Reims Champagne-Ardenne, ANSES, EA4688 – USC [Transmission vectorielle et épidémiosurveillance de maladies parasitaires (VECPAR)], 51, rue Cognacq-Jay, 51096 Reims Cedex, France
                [ ]Departamento de Epidemiologia, Faculdade de Saúde Pública, Universidade de São Paulo, SP 01246-904 São Paulo, Brazil
                [ ]Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12735 Twinbrook Parkway, Rockville, MD 20852 USA
                [ ]c/o Istituto Superiore di Sanità, Rome, Italy
                [ ]Eck Institute for Global Health, Department of Biological Sciences, University of Notre Dame, Notre Dame IN, USA
                [ ]ISGlobal, Barcelona Ctr. Int. Health Res. (CRESIB), Hospital Clínic, Universitat de Barcelona, Barcelona, E-08036 Spain
                [ ]Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT UK
                [ ]National Institute of Tropical Medicine-MOH, CONICET, Neuquen y Jujuy s/n, 3370, Puerto Iguazu, Argentina
                [ ]Biomedical Sciences Institute, Universidade de São Paulo, SP, São Paulo, Brazil
                [ ]Laboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, RJ, Brazil
                [ ]Kuvin Center for the study of Infectious & Tropical Diseases, Institute of Medical Research Israel-Canada/ Faculty of Medicine, Hebrew University of Jerusalem, Ein Kerem, Jerusalem, 91120 Israel
                Article
                712
                10.1186/s13071-015-0712-x
                4352286
                25885217
                37912685-095a-4622-9104-778adb589fc5
                © Bates et al. licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 19 December 2014
                : 3 February 2015
                Categories
                Review
                Custom metadata
                © The Author(s) 2015

                Parasitology
                phlebotomine sand flies,human leishmaniasis,vector control,leishmaniasis control,isops

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