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      Minimally invasive microbiopsies: a novel sampling method for identifying asymptomatic, potentially infectious carriers of Leishmania donovani

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          Highlights

          • Microbiopsy devices were designed to assess the infectiousness of asymptomatic Leishmania donovani carriers.

          • The microbiopsy devices sample both skin tissues and blood, as do pool-feeding phlebotomine sand flies.

          • Devices were tested on human volunteers in Ethiopia and proven effective, surpassing the sensitivity of finger-pricks.

          Abstract

          Visceral leishmaniasis (VL) is a potentially lethal, sand fly-borne disease caused by protozoan parasites belonging to the Leishmania donovani species complex. There are several adequate methods for diagnosing VL, but the majority of infected individuals remain asymptomatic, comprising potential parasite reservoirs for transmission of the disease. The gold standard for assessing host infectiousness to biting vector insects is xenodiagnosis (i.e. scoring infection rates among insectary-reared insects that had fed on humans suspected of being infected). However, when it comes to sand flies and leishmaniasis, xenodiagnosis is an intricate operation burdened by logistical hurdles and ethical concerns that prevent its effective application for mass screening of widely dispersed communities, particularly in rural regions of underdeveloped countries. Minimally invasive microbiopsy (MB) devices were designed to penetrate the skin to a depth of ∼200 µm and absorb blood as well as skin cell lysates, mimicking the mode by which phlebotomine sand flies acquire blood meals, as well as their composition. MBs taken from 137 of 262 volunteers, living in endemic VL foci in Ethiopia, detected Leishmania parasites that could potentially be imbibed by feeding sand flies. Although the volume of MBs was 10-fold smaller than finger-prick blood samples, Leishmania DNA detection rates from MBs were significantly higher, implying that skin, more often than blood, was the source of parasites. Volunteers with histories of VL were almost as likely as healthy volunteers to test positive by MBs (southern Ethiopian focus: 95% CI: 0.35–2.59, P = 1.0. northern Ethiopian focus 0.87: 95% CI: 0.22–3.76, P = 1), suggesting the importance of asymptomatic patients as reservoirs of L. donovani. Minimally invasive, painless MBs should be considered for reliably and efficiently evaluating both L. donovani infection rates among large numbers of asymptomatic carriers and their infectiousness to blood-feeding sand flies.

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          Most cited references30

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          Visceral leishmaniasis: what are the needs for diagnosis, treatment and control?

          Visceral leishmaniasis (VL) is a systemic protozoan disease that is transmitted by phlebotomine sandflies. Poor and neglected populations in East Africa and the Indian sub-continent are particularly affected. Early and accurate diagnosis and treatment remain key components of VL control. In addition to improved diagnostic tests, accurate and simple tests are needed to identify treatment failures. Miltefosine, paromomycin and liposomal amphotericin B are gradually replacing pentavalent antimonials and conventional amphotericin B as the preferred treatments in some regions, but in other areas these drugs are still being evaluated in both mono- and combination therapies. New diagnostic tools and new treatment strategies will only have an impact if they are made widely available to patients.
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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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              The early interaction of Leishmania with macrophages and dendritic cells and its influence on the host immune response

              The complicated interactions between Leishmania and the host antigen-presenting cells (APCs) have fundamental effects on the final outcome of the disease. Two major APCs, macrophages and dendritic cells (DCs), play critical roles in mediating resistance and susceptibility during Leishmania infection. Macrophages are the primary resident cell for Leishmania: they phagocytose and permit parasite proliferation. However, these cells are also the major effector cells to eliminate infection. The effective clearance of parasites by macrophages depends on activation of appropriate immune response, which is usually initiated by DCs. Here, we review the early interaction of APCs with Leishmania parasites and how these interactions profoundly impact on the ensuing adaptive immune response. We also discuss how the current knowledge will allow further refinement of our understanding of the interplay between Leishmania and its hosts that leads to resistance or susceptibility.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol
                Int. J. Parasitol
                International Journal for Parasitology
                Elsevier Science
                0020-7519
                1879-0135
                1 September 2017
                September 2017
                : 47
                : 10-11
                : 609-616
                Affiliations
                [a ]Department of Microbiology and Molecular Genetics, The Institute for Medical Research Israel-Canada (IMRIC), The Kuvin Centre for the Study of Infectious and Tropical Diseases, The Hebrew University – Hadassah Medical School, The Hebrew University of Jerusalem, 91120, Israel
                [b ]Department of Biostatistics, School of Public Health, Yale University, 60 College Street, New Haven, CT 06520, USA
                [c ]Department of Microbiology, Immunology & Parasitology, Faculty of Medicine, Addis Ababa University, P.O. Box 9086, Addis Ababa, Ethiopia
                [d ]Dermatology Research Centre, The University of Queensland School of Medicine, Translational Research Institute, Brisbane, QLD 4012, Australia
                Author notes
                [* ]Corresponding author at: Department of Microbiology and Molecular Genetics, The Institute for Medical Research Israel-Canada (IMRIC), The Kuvin Centre for the Study of Infectious and Tropical Diseases, Botnar Building, Floor -1, Room: A003, The Hebrew University – Hadassah Medical School, The Hebrew University of Jerusalem, 91120, Israel.Department of Microbiology and Molecular GeneticsThe Institute for Medical Research Israel-Canada (IMRIC)The Kuvin Centre for the Study of Infectious and Tropical DiseasesBotnar Building, Floor -1, Room: A003The Hebrew University – Hadassah Medical SchoolThe Hebrew University of Jerusalem91120Israel alonw@ 123456ekmd.huji.ac.il
                Article
                S0020-7519(17)30104-2
                10.1016/j.ijpara.2017.02.005
                5596977
                28455239
                4dbf9e0c-a3d7-4c4c-a65e-801ffc9db838
                © 2017 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 6 October 2016
                : 20 February 2017
                : 24 February 2017
                Categories
                Article

                Parasitology
                asymptomatic carriers,leishmania donovani,microbiopsy,phlebotomine sand flies,visceral leishmaniasis,xenodiagnosis

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