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      A field study of the survival and dispersal pattern of Lutzomyia longipalpis in an endemic area of visceral leishmaniasis in Brazil

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          Abstract

          Zoonotic Visceral leishmaniasis (ZVL) is a neglected tropical disease that in the Americas is caused by the infection of Leishmania infantum and the domestic dog ( Canis familiaris) is the main parasite reservoir in urban areas. The parasite is mainly transmitted by populations of the sibling species Lutzomyia longipalpis that has been spreading in countries including Brazil, Argentina, Paraguay and more recently Uruguay. Although bionomic parameters such as population survival and the duration of the gonotrophic cycle are critical in evaluating vector capacity, field studies have rarely been applied to sand fly populations. The present study sought to evaluate basic bionomic parameters related to the vectorial capacity of the (S)-9-methylgermacrene-B population of the Lu. longipalpis complex in a visceral leishmaniasis area of Sao Paulo state. The daily survival rate, the duration of the gonotrophic cycle and the dispersal pattern were evaluated through the mark- release-recapture method. A total of 1,547 males and 401 females were marked and released in five experiments carried out between February 2013 and February 2014. The higher recapture rates occurred within 100 meters of the release point and the estimated daily survival rates varied between 0.69 and 0.89 for females and between 0.69 and 0.79 for males. The minimum duration of the gonotrophic cycle observed was five days. The absolute population size, calculated ranged from 900 to 4,857 females and from 2,882 to 9,543 males. Our results demonstrate a high survival rate of this vector population and low dispersal that could be associated with the presence of all necessary conditions for its establishment and maintenance in the peridomiciles of this area. Our findings contribute to the basic data necessary for the understanding of ZVL dynamics and the evaluation of the implementation of prevention and control measures.

          Author summary

          American Visceral leishmaniasis (VL) is an anthropozoonosis resulting from infection by Leishmania infantum mainly transmitted by the bite of females of the sand fly Lutzomyia longipalpis which feed mainly on domestic dogs. It is a serious tropical disease that in some countries has spread in association with several factors such as human migration, precarious urbanization and vector adaptation to urban areas. In Brazil, although control measures such as the elimination of infected dogs, the application of residual insecticide and environmental management have been applied by the health authorities, however, they have not resulted in any significant reduction in VL incidence. The knowledge of bionomic parameters of vector populations is critical for the understanding of the transmission dynamic of VL and to evaluate prevention and control measures. Therefore, in the present study we applied the mark-release-recapture (MRR) method to evaluate under field conditions some basic bionomic parameters of a population of the Lutzomyia longipalpis complex. Our findings demonstrate a high survival rate of this vector and a low population dispersal. These results suggest that measures applied to dog populations to prevent sand fly bites could contribute to the reduction of the surviving vector population and indirectly to the reduction of the host biting rate. Additionally, the low dispersal suggests that environmental management could contribute to the reduction of vector density. Our data serve as the first estimates of vector survival rates of populations of the sibling species Lu. longipalpis under natural conditions and could be applied in the evaluation of prevention and control measures.

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          Most cited references47

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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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              Landscape epidemiology of vector-borne diseases.

              Landscape epidemiology describes how the temporal dynamics of host, vector, and pathogen populations interact spatially within a permissive environment to enable transmission. The spatially defined focus, or nidus, of transmission may be characterized by vegetation as well as by climate, latitude, elevation, and geology. The ecological complexity, dimensions, and temporal stability of the nidus are determined largely by pathogen natural history and vector bionomics. Host populations, transmission efficiency, and therefore pathogen amplification vary spatially, thereby creating a heterogeneous surface that may be defined by remote sensing and statistical tools. The current review describes the evolution of landscape epidemiology as a science and exemplifies selected aspects by contrasting the ecology of two different recent disease outbreaks in North America caused by West Nile virus, an explosive, highly virulent mosquito-borne virus producing ephemeral nidi, and Borrelia burgdorferi, a slowly amplifying chronic pathogen producing semipermanent nidi.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                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
                2 April 2018
                April 2018
                : 12
                : 4
                : e0006333
                Affiliations
                [1 ] Departamento de Epidemiologia, Faculdade de Saúde Pública, Universidade de São Paulo, São Paulo, Brasil
                [2 ] Laboratório de Parasitoses por flagelados, Superintendência de Controle de Endemias, Secretaria de Estado da Saúde, Mogi Guaçu, São Paulo, Brasil
                National Institutes of Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-2105-7941
                Article
                PNTD-D-17-01816
                10.1371/journal.pntd.0006333
                5880336
                29608563
                e612c2e9-01ac-412b-b737-1f9859c9bd78
                © 2018 Galvis-Ovallos 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 November 2017
                : 21 February 2018
                Page count
                Figures: 2, Tables: 4, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2012/03751-4
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001807, Fundação de Amparo à Pesquisa do Estado de São Paulo;
                Award ID: 2011/23541-1
                Award Recipient :
                This study was supported by the São Paulo Research Foundation - Brazil (FAPESP, to EABG 212/03751-4 and Fellowship to FG-O 2011/23541-1). 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
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Sand Flies
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Sand Flies
                People and places
                Geographical locations
                South America
                Brazil
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Kala-Azar
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Kala-Azar
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                Kala-Azar
                Medicine and Health Sciences
                Infectious Diseases
                Vector-Borne Diseases
                Earth Sciences
                Geography
                Geographic Areas
                Urban Areas
                Custom metadata
                All relevant data are within the paper.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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