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      Leishmania naiffi and  lainsoni in French Guiana: Clinical features and phylogenetic variability

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          Abstract

          In French Guiana, five species are associated with Cutaneous Leishmaniasis (CL). Though infections with Leishmania guyanensis, L. (V. ) braziliensis and L. (L. ) amazonensis have been extensively described, there are few available clinical and genetic data on L. (V. ) lainsoni and L. (V. ) naiffi. We determined the clinical and epidemiological features of all cases of CL due to L. (V. ) naiffi and L. (V. ) lainsoni diagnosed in French Guiana between 2003 and 2019. Phylogenetic analysis was performed by sequencing a portion of HSP70 and cyt b genes. Five cases of L. naiffi and 25 cases of L. lainsoni were reported. Patients infected by L. (V. ) lainsoni were usually infected on gold camps, mostly along the Maroni river (60%), while L. naiffi was observed in French patients infected on the coast (100%). A high number of pediatric cases (n = 5; 20%) was observed for L. (V. ) lainsoni. A mild clinical course was observed for all cases of L. (V. ) naiffi. HSP70 and cyt b partial nucleotide sequence analysis revealed different geographical clusters within L. (V. ) naiffi and L. (V. ) lainsoni but no association were found between phylogenetic and clinical features. Our data suggest distinct socio-epidemiological features for these two Leishmania species. Patients seem to get infected with L. (V. ) naiffi during leisure activities in anthropized coastal areas, while L. (V. ) lainsoni shares common features with L. (V. ) guyanensis and braziliensis and seems to be acquired during professional activities in primary forest regions. Phylogenetic analysis has provided information on the intraspecific genetic variability of L. (V. ) naiffi and L. (V. ) lainsoni and how these genotypes are distributed at the geographic level.

          Author summary

          Cutaneous leishmaniasis is a parasitic disease affecting at least 12 million people in 96 countries. In French Guiana, five species of Leishmania are involved in human disease: Leishmania (V. ) guyanensis, Leishmania (V. ) braziliensis and Leishmania (L. ) amazonensis are common and have been extensively studied. Leishmania (V. ) lainsoni and Leishmania (V. ) naiffi are less frequent and very few data are available on the patients infected by these species. In this study, we identified five cases of human patients infected by L. (V. ) naiffi and 25 cases of L. (V. ) lainsoni. Patients infected by L. (V. ) lainsoni were usually god miners infected in the rainforest, while L. naiffi was observed in patients infected on the anthropized coast of French Guiana. L. naiffi was associated with mild lesions. Pentamidine was an efficient treatment for most cases of both species.

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          Most cited references57

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          Culture-independent species typing of neotropical Leishmania for clinical validation of a PCR-based assay targeting heat shock protein 70 genes.

          PCR-restriction fragment length polymorphism analysis of heat shock protein 70 genes discriminates most neotropical Leishmania species, as well as Trypanosoma cruzi. The assay, combined with capillary electrophoresis in a microchip device, may be applied directly on clinical samples with a high sensitivity, hence supporting clinical and epidemiological monitoring of leishmaniasis.
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            Phylogeny of Leishmania species based on the heat-shock protein 70 gene.

            The 70kDa heat-shock protein (HSP70) is conserved across prokaryotes and eukaryotes, and the protein as well as its encoding gene have been applied in phylogenetic studies of different parasites. In spite of the frequent use of New World Leishmania species identification on the basis of restriction fragment length polymorphisms (RFLP) in the hsp70 gene, it was never sequenced extensively for studying evolutionary relationships. To fill this void we determined the nucleotide sequence of an 1380bp fragment of the coding region commonly used in RFLP analysis, from 43 isolates and strains of different geographic origins. Combination with previously determined sequences amounted to a phylogenetic analysis including 52 hsp70 sequences representing 17 species commonly causing leishmaniasis both in the New and Old World. The genus Leishmania formed a monophyletic group with three distinct subgenera L. (Leishmania), L. (Viannia), and L. (Sauroleishmania). The obtained phylogeny supports the following eight species: L. (L.) donovani, L. (L.) major, L. (L.) tropica, L. (L.) mexicana, L. (V.) lainsoni, L. (V.) naiffi, L. (V.) guyanensis and L. (V.) braziliensis, in some of which subspecies can be recognized: L. (L.) donovani infantum, L. (V.) guyanensis panamensis, and L. (V.) braziliensis peruviana. The currently recognized L. (L.) aethiopica, L. (L.) garnhami, and L. (L.) amazonensis did not form monophyletic clusters. These findings are discussed in relation to results from other genes and proteins, which have to be integrated in order to build a genetically supported taxonomy for the entire genus.
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              Immunopathogenic competences of Leishmania (V.) braziliensis and L. (L.) amazonensis in American cutaneous leishmaniasis.

              The immunopathogenic competences of Leishmania (V.) braziliensis and L. (L.) amazonensis were reviewed in the light of more recent features found in the clinical and immunopathological spectrum of American cutaneous leishmaniasis. It was shown a dichotomy in the interaction between these Leishmania species and human T-cell immune response; while L. (V.) braziliensis shows a clear tendency to lead infection from the localized cutaneous leishmaniasis (LCL), a moderate T-cell hypersensitivity form at the centre of the spectrum, toward to the mucocutaneous leishmaniasis (MCL) at the T-cell hypersensitivity pole and with a prominent Th1-type immune response, L. (L.) amazonensis shows an opposite tendency, leading infection to the anergic diffuse cutaneous leishmaniasis (ADCL) at the T-cell hyposensitivity pole and with a marked Th2-type immune response. Between the central LCL and the two polar MCL and ADCL, the infection can present an intermediary form known as borderline disseminated cutaneous leishmaniasis, characterized by an incomplete inhibition of T-cell hypersensitivity but with a evident supremacy of Th1 over Th2 immune response (Th1 > or = Th2). These are probably the main immunopathogenic competences of L. (V.) braziliensis and L. (L.) amazonensis regarding the immune response dichotomy that modulates human infection outcome by these Leishmania parasites.
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                Author and article information

                Contributors
                Role: InvestigationRole: Writing – original draft
                Role: Investigation
                Role: Investigation
                Role: Data curationRole: InvestigationRole: Resources
                Role: Supervision
                Role: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ValidationRole: 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
                14 August 2020
                August 2020
                : 14
                : 8
                : e0008380
                Affiliations
                [1 ] Service de Dermatologie, Hôpital Andrée Rosemon, Cayenne, French Guiana
                [2 ] Equipe EA3593, Ecosystèmes Amazoniens et Pathologie Tropicale, Université de la Guyane, Cayenne, French Guiana
                [3 ] Centre National de Référence des Leishmanioses, laboratoire associé, Hôpital Andrée Rosemon, Cayenne, French Guiana
                [4 ] Laboratoire Hospitalo-Universitaire de Parasitologie-Mycologie, Hôpital Andrée Rosemon, Cayenne, French Guiana
                Institut Pasteur de Tunis, TUNISIA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-3695-6824
                Article
                PNTD-D-20-00019
                10.1371/journal.pntd.0008380
                7449503
                32797078
                1b51d467-db71-4e95-bfab-9a50aad40f3f
                © 2020 Ducharme 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
                : 18 January 2020
                : 11 May 2020
                Page count
                Figures: 3, Tables: 2, Pages: 17
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Leishmania
                People and places
                Geographical locations
                South America
                Brazil
                Medicine and Health Sciences
                Clinical Medicine
                Signs and Symptoms
                Lesions
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Sequencing Techniques
                Nucleotide Sequencing
                Research and Analysis Methods
                Molecular Biology Techniques
                Sequencing Techniques
                Nucleotide Sequencing
                Earth Sciences
                Geography
                Regional Geography
                Geographical Regions
                Coastal Regions
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Pediatric Infections
                Medicine and Health Sciences
                Pediatrics
                Pediatric Infections
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-08-26
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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