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Advances in Leishmania Research: From Basic Parasite Biology to Disease Control

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Parasitology".

Deadline for manuscript submissions: closed (31 August 2022) | Viewed by 21389

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Prof. Dr. Anabela Cordeiro da Silva

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I3S-Instituto de Investigação e Inovação em Saúde and Faculdade de Farmácia, Universidade do Porto, 4050-313 Porto, Portugal
Interests: leishmaniasis; host–parasite interactions; vaccine development; biomarker development; virulence factors

Dr. Luís Cardoso

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Department of Veterinary Sciences, School of Agrarian and Veterinary Sciences, Veterinary and Animal Research Center (CECAV), University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal
Interests: veterinary sciences; parasitology; parasitic diseases; epidemiology; One Health
Special Issues, Collections and Topics in MDPI journals

Dr. Nuno Santarém

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Institute for Research and Innovation in Health (i3S), University of Porto, 4200-135 Porto, Portugal
Interests: leishmaniasis; host-pathogen interaction, extra-cellular vesicles, drug development and disease management (diagnosis)
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Leishmaniases are a group of vector-borne diseases caused by more than 20 Leishmania species. There are three main forms of the disease: cutaneous leishmaniasis (CL), visceral leishmaniasis (VL), and mucocutaneous leishmaniasis. More than 1 billion people live in areas endemic for leishmaniasis and are at risk of infection. An estimated 30,000 new cases of VL and more than 1 million new cases of CL occur annually. Considering the inexistence of vaccines in humans, disease control requires active treatment and prophylaxis. Unfortunately, the available therapeutic options and disease management is suboptimal, contributing to a yearly death toll of more than 20,000. Although VL is considered the most severe form of disease, each form presents specific unmet challenges that can only be overcome by a better understanding of parasite biology, ecology, and disease process.

In this Special Issue of Microorganisms, we invite you to send original contributions in Leishmania research on basic parasite biology, drug and vaccine development, host–parasite interactions, epidemiology, and leishmaniasis control.

Prof. Dr. Anabela Cordeiro da Silva
Prof. Dr. Luís Cardoso
Dr. Nuno Santarém
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

leishmaniasis
host–parasite interactions
anti-trypanomatid drug development
vaccine development
biomarker development
virulent factors
canine leishmaniosis

Published Papers (11 papers)

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Editorial

Jump to: Research, Review

4 pages, 233 KiB

Open AccessEditorial

Advances in Leishmania Research: From Basic Parasite Biology to Disease Control

by Nuno Santarém, Luís Cardoso and Anabela Cordeiro-da-Silva

Microorganisms 2023, 11(3), 696; https://doi.org/10.3390/microorganisms11030696 - 08 Mar 2023

Viewed by 941

Abstract

The genus Leishmania (Trypanosomatida: Trypanosomatidae) currently comprises just over 50 species, of which about 20 cause several syndromes in humans, collectively known as leishmaniasis or “leishmaniases” [...] Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

Research

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14 pages, 1477 KiB

Open AccessArticle

Comparative Genomic Analyses of New and Old World Viscerotropic Leishmanine Parasites: Further Insights into the Origins of Visceral Leishmaniasis Agents

by Fernando Tobias Silveira, Edivaldo Costa Sousa Junior, Rodrigo Vellasco Duarte Silvestre, Thiago Vasconcelos dos Santos, Wilfredo Sosa-Ochoa, Concepción Zúniga Valeriano, Patrícia Karla Santos Ramos, Samir Mansour Moraes Casseb, Luciana Vieira do Rêgo Lima, Marliane Batista Campos, Vania Lucia da Matta, Claudia Maria Gomes, Gabriela V. Araujo Flores, Carmen M. Sandoval Pacheco, Carlos Eduardo Corbett and Márcia Dalastra Laurenti

Microorganisms 2023, 11(1), 25; https://doi.org/10.3390/microorganisms11010025 - 21 Dec 2022

Cited by 5 | Viewed by 1803

Abstract

Visceral leishmaniasis (VL), also known as kala-azar, is an anthropozoonotic disease affecting human populations on five continents. Aetiologic agents belong to the Leishmania (L.) donovani complex. Until the 1990s, three leishmanine parasites comprised this complex: L. (L.) donovani Laveran & Mesnil 1903, L. (L.) infantum Nicolle 1908, and L. (L.) chagasi Lainson & Shaw 1987 (=L. chagasi Cunha & Chagas 1937). The VL causal agent in the New World (NW) was previously identified as L. (L.) chagasi. After the development of molecular characterization, however, comparisons between L. (L.) chagasi and L. (L.) infantum showed high similarity, and L. (L.) chagasi was then regarded as synonymous with L. (L.) infantum. It was, therefore, suggested that L. (L.) chagasi was not native to the NW but had been introduced from the Old World by Iberian colonizers. However, in light of ecological evidence from the NW parasite’s enzootic cycle involving a wild phlebotomine vector (Lutzomyia longipalpis) and a wild mammal reservoir (the fox, Cerdocyon thous), we have recently analyzed by molecular clock comparisons of the DNA polymerase alpha subunit gene the whole-genome sequence of L. (L.) infantum chagasi of the most prevalent clinical form, atypical dermal leishmaniasis (ADL), from Honduras (Central America) with that of the same parasite from Brazil (South America), as well as those of L. (L.) donovani (India) and L. (L.) infantum (Europe), which revealed that the Honduran parasite is older ancestry (382,800 ya) than the parasite from Brazil (143,300 ya), L. (L.) donovani (33,776 ya), or L. (L.) infantum (13,000 ya). In the present work, we have now amplified the genomic comparisons among these leishmanine parasites, exploring mainly the variations in the genome for each chromosome, and the number of genomic SNPs for each chromosome. Although the results of this new analysis have confirmed a high genomic similarity (~99%) among these parasites [except L. (L.) donovani], the Honduran parasite revealed a single structural variation on chromosome 17, and the highest frequency of genomic SNPs (more than twice the number seen in the Brazilian one), which together to its extraordinary ancestry (382,800 ya) represent strong evidence that L. (L.) chagasi/L. (L.) infantum chagasi is, in fact, native to the NW, and therefore with valid taxonomic status. Furthermore, the Honduran parasite, the most ancestral viscerotropic leishmanine parasite, showed genomic and clinical taxonomic characteristics compatible with a new Leishmania species causing ADL in Central America. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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16 pages, 827 KiB

Open AccessArticle

Serological and Molecular Survey of Leishmania infantum in a Population of Iberian Lynxes (Lynx pardinus)

by Clara M. Lima, Nuno Santarém, Nuno Costa Neves, Pedro Sarmento, Carlos Carrapato, Rita de Sousa, Luís Cardoso and Anabela Cordeiro-da-Silva

Microorganisms 2022, 10(12), 2447; https://doi.org/10.3390/microorganisms10122447 - 11 Dec 2022

Cited by 3 | Viewed by 1735

Abstract

Leishmania infantum, the sand fly-transmitted protozoan parasite responsible for leishmaniasis in humans, dogs, and cats, is endemic in the Iberian Peninsula. However, the impact of L. infantum infection on the conservation of the endangered Iberian lynx (Lynx pardinus) is unknown. Herein, we describe for the first time the occurrence of L. infantum infection among a population of reintroduced and wild-born L. pardinus living in the Portuguese Guadiana Valley Park. The presence of infection was addressed by molecular detection of Leishmania kinetoplast DNA (kDNA) in 35 lynxes, with further confirmation of L. infantum species performed by an internally transcribed spacer (ITS)-1 sequencing. Eight blood samples were positive for kDNA, and ITS-1 sequencing confirmed the presence of L. infantum in two of those samples. Exposure to Leishmania was screened in a group of 36 lynxes using an immunofluorescence antibody test (IFAT) and a multi-antigen enzyme-linked immunosorbent assay (ELISA), using SPLA, rK39, and CPX as Leishmania-specific antigens. Four animals presented a positive IFAT at a dilution of 1:40. Eight samples were considered seropositive to all ELISA Leishmania-specific antigens. Agreement between PCR, IFAT, and all ELISA antigens was found for 1 in 27 samples. These results highlight the susceptibility of autochthonous L. pardinus to L. infantum infection. Further investigation is required to assess the impact of L. infantum infection on this wild species conservation. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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13 pages, 1478 KiB

Open AccessCommunication

Identification of Leishmania infantum Epidemiology, Drug Resistance and Pathogenicity Biomarkers with Nanopore Sequencing

by Joan Martí-Carreras, Marina Carrasco, Marcel Gómez-Ponce, Marc Noguera-Julián, Roser Fisa, Cristina Riera, Maria Magdalena Alcover, Xavier Roura, Lluís Ferrer and Olga Francino

Microorganisms 2022, 10(11), 2256; https://doi.org/10.3390/microorganisms10112256 - 14 Nov 2022

Cited by 4 | Viewed by 1890

Abstract

The emergence of drug-resistant strains of the parasite Leishmania infantum infecting dogs and humans represents an increasing threat. L. infantum genomes are complex and unstable with extensive structural variations, ranging from aneuploidies to multiple copy number variations (CNVs). These CNVs have recently been validated as biomarkers of Leishmania concerning virulence, tissue tropism, and drug resistance. As a proof-of-concept to develop a novel diagnosis platform (LeishGenApp), four L. infantum samples from humans and dogs were nanopore sequenced. Samples were epidemiologically typed within the Mediterranean L. infantum group, identifying members of the JCP5 and non-JCP5 subgroups, using the conserved region (CR) of the maxicircle kinetoplast. Aneuploidies were frequent and heterogenous between samples, yet only chromosome 31 tetrasomy was common between all the samples. A high frequency of aneuploidies was observed for samples with long passage history (MHOM/TN/80/IPT-1), whereas fewer were detected for samples maintained in vivo (MCRI/ES/2006/CATB033). Twenty-two genes were studied to generate a genetic pharmacoresistance profile against miltefosine, allopurinol, trivalent antimonials, amphotericin, and paromomycin. MHOM/TN/80/IPT-1 and MCRI/ES/2006/CATB033 displayed a genetic profile with potential resistance against miltefosine and allopurinol. Meanwhile, MHOM/ES/2016/CATB101 and LCAN/ES/2020/CATB102 were identified as potentially resistant against paromomycin. All four samples displayed a genetic profile for resistance against trivalent antimonials. Overall, this proof-of-concept revealed the potential of nanopore sequencing and LeishGenApp for the determination of epidemiological, drug resistance, and pathogenicity biomarkers in L. infantum. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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15 pages, 1707 KiB

Open AccessArticle

Use of Antigen Combinations to Address Complex Leishmania-Seropositivity Patterns in Dogs Living in Canine Leishmaniosis Endemic Regions of Portugal

by Carla Silva Lima, Sofia Esteves, Inês Costa, Hugo Brancal, Clara Lima, Célia Amorim, Luís Cardoso, Nuno Santarém and Anabela Cordeiro-da-Silva

Microorganisms 2022, 10(10), 2018; https://doi.org/10.3390/microorganisms10102018 - 12 Oct 2022

Cited by 3 | Viewed by 1261

Abstract

Canine leishmaniosis (CanL) is a vector-borne disease caused by Leishmania infantum. Infection in dogs can result in a disease with non-specific clinical signs or in a subclinical condition. Infection diagnosis is crucial to guide public health measures considering the zoonotic potential of L. infantum. Serological approaches to detect infection with a reduced antigen panel potentially limit the quality of the information obtained. To evaluate the impact of using distinct antigens in a serological survey, a cohort with 390 dogs from endemic regions in Portugal was subjected to a serological evaluation using ELISA and DAT. Using ELISA, six Leishmania-specific antigens in conjunction with a non-related antigen, Escherichia coli soluble antigens, were evaluated. The global seroprevalence was 10.5% for DAT and 15.4 to 23.1% for ELISA, depending on the antigen for the latter. Still, only 8.2% of the animals were seropositive to all Leishmania-specific antigens. Importantly, a further 31.0% presented antigen-dependent seropositivity. Considering this observation, a serological score system was proposed and validated to address the complex serology results. With this system, the overall dog seropositivity was 26.9%. This work highlights the limitations of single-antigen serological surveys and presents an approach that might contribute to the establishment of CanL-specific serological profiles. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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14 pages, 2497 KiB

Open AccessArticle

First Report of Two Jaculus Rodents as Potential Reservoir Hosts of Leishmania Parasites in Tunisia

by Wissem Ghawar, Melek Chaouch, Afif Ben Salah, Mohamed Ali Snoussi, Sadok Salem, Ghassen Kharroubi, Said Chouchen, Amor Bouaoun, Dhafer Laouini, Jihene Bettaieb and Souha Ben Abderrazak

Microorganisms 2022, 10(8), 1502; https://doi.org/10.3390/microorganisms10081502 - 25 Jul 2022

Cited by 1 | Viewed by 1443

Abstract

This study shows, for the first time, natural Leishmania infection among Jaculus spp. in an endemic region of Tataouine, South Tunisia. To better characterize the transmission cycles in this complex focus of mixed transmission, Leishmania detection and species identification were performed by direct examination, internal transcribed spacer-1 (ITS1)-PCR-restriction fragment length polymorphism (RFLP), and sequencing of Jaculus (J.) jaculus (Linnaeus, 1758) and J. hirtipes (Lichtenstein, 1823) rodent species, which are frequently encountered in this area. Leishmania parasites were observed in 19 (41.3%) smears, while DNA parasites were detected in 28 (60.9%) Jaculus spp. spleens; among them, 12 (54.5%) were from 22 J. jaculus individuals and 16 (66.7%) were from 24 J. hirtipes individuals. Leishmania parasites were confirmed as Leishmania (L.) killicki (syn. L. tropica) in two J. hirtipes individuals (4.3%) and L. major (n = 24; 52.2%) in 10 J. jaculus and 14 J. hirtipes individuals. This finding represents the first evidence of natural infection with Leishmania parasites in rodents belonging to the Jaculus genus, providing the rationale to consider them as potential reservoir hosts of Old World Leishmania parasites in Tunisia and North Africa. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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19 pages, 2036 KiB

Open AccessArticle

Transcriptome Analysis of Intracellular Amastigotes of Clinical Leishmania infantum Lines from Therapeutic Failure Patients after Infection of Human Macrophages

by Raquel García-Hernández, Ana Perea-Martínez, José Ignacio Manzano, Laura C. Terrón-Camero, Eduardo Andrés-León and Francisco Gamarro

Microorganisms 2022, 10(7), 1304; https://doi.org/10.3390/microorganisms10071304 - 27 Jun 2022

Cited by 1 | Viewed by 1980

Abstract

Leishmaniasis is considered to be one of the most neglected tropical diseases affecting humans and animals around the world. Due to the absence of an effective vaccine, current treatment is based on chemotherapy. However, the continuous appearance of drug resistance and therapeutic failure (TF) lead to an early obsolescence of treatments. Identification of the factors that contribute to TF and drug resistance in leishmaniasis will constitute a useful tool for establishing future strategies to control this disease. In this manuscript, we evaluated the transcriptomic changes in the intracellular amastigotes of the Leishmania infantum parasites isolated from patients with leishmaniasis and TF at 96 h post-infection of THP-1 cells. The adaptation of the parasites to their new environment leads to expression alterations in the genes involved mainly in the transport through cell membranes, energy and redox metabolism, and detoxification. Specifically, the gene that codes for the prostaglandin f2α synthase seems to be relevant in the pathogenicity and TF since it appears substantially upregulated in all the L. infantum lines. Overall, our results show that at the late infection timepoint, the transcriptome of the parasites undergoes significant changes that probably improve the survival of the Leishmania lines in the host cells, contributing to the TF phenotype as well as drug therapy evasion. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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16 pages, 2777 KiB

Open AccessArticle

Leishmania infantum Infection of Primary Human Myeloid Cells

by Morgane Picard, Calaiselvy Soundaramourty, Ricardo Silvestre, Jérôme Estaquier and Sónia André

Microorganisms 2022, 10(6), 1243; https://doi.org/10.3390/microorganisms10061243 - 17 Jun 2022

Cited by 3 | Viewed by 1814

Abstract

Circulating phagocytic cells often serve as cellular targets for a large number of pathogens such as Leishmania parasites. Studying primary human cells in an infectious context requires lengthy procedures for cell isolation that may affect the analysis performed. Using whole blood and a no-lyse and no-wash flow cytometric assay (NoNo assay), we monitored the Leishmania infantum infection of primary human cells. We demonstrated, using fluorescent parasites, that among monocyte cell populations, L. infantum preferentially infects classical (CD14⁺CD16⁻) and intermediate (CD14⁺CD16⁺) primary human monocytes in whole blood. Because classical monocytes are the preponderant population, they represent the larger L. infantum reservoir. Moreover, we also found that, concomitantly to monocyte infection, a subset of PMNs is infected early in whole blood. Of interest, in whole blood, PMNs are less infected compared to classical monocytes. Overall, by using this NoNo assay, we provided a novel avenue in our understanding of host–leishmania interactions. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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17 pages, 2297 KiB

Open AccessArticle

Protective Efficacy in a Hamster Model of a Multivalent Vaccine for Human Visceral Leishmaniasis (MuLeVaClin) Consisting of the KMP11, LEISH-F3+, and LJL143 Antigens in Virosomes, Plus GLA-SE Adjuvant

by Laura Fernández, Jose Carlos Solana, Carmen Sánchez, Mª Ángeles Jiménez, Jose M. Requena, Rhea Coler, Steven G. Reed, Jesus G. Valenzuela, Shaden Kamhawi, Fabiano Oliveira, Epifanio Fichera, Reinhard Glueck, Maria Elena Bottazzi, Gaurav Gupta, Pedro Cecilio, Begoña Pérez-Cabezas, Anabela Cordeiro-da-Silva, Luigi Gradoni, Eugenia Carrillo and Javier Moreno

Microorganisms 2021, 9(11), 2253; https://doi.org/10.3390/microorganisms9112253 - 29 Oct 2021

Cited by 9 | Viewed by 3057

Abstract

Visceral leishmaniasis (VL) is the most severe clinical form of leishmaniasis, fatal if untreated. Vaccination is the most cost-effective approach to disease control; however, to date, no vaccines against human VL have been made available. This work examines the efficacy of a novel vaccine consisting of the Leishmania membrane protein KMP11, LEISH-F3+ (a recombinant fusion protein, composed of epitopes of the parasite proteins nucleoside hydrolase, sterol-24-c-methyltransferase, and cysteine protease B), and the sand fly salivary protein LJL143, in two dose ratios. The inclusion of the TLR4 agonist GLA-SE as an adjuvant, and the use of virosomes (VS) as a delivery system, are also examined. In a hamster model of VL, the vaccine elicited antigen-specific immune responses prior to infection with Leishmania infantum. Of note, the responses were greater when higher doses of KMP11 and LEISH-F3+ proteins were administered along with the GLA-SE adjuvant and/or when delivered within VS. Remarkably, hamsters immunized with the complete combination (i.e., all antigens in VS + GLA-SE) showed significantly lower parasite burdens in the spleen compared to those in control animals. This protection was underpinned by a more intense, specific humoral response against the KMP11, LEISH-F3+, and LJL143 antigens in vaccinated animals, but a significantly less intense antibody response to the pool of soluble Leishmania antigens (SLA). Overall, these results indicate that this innovative vaccine formulation confers protection against L. infantum infection, supporting the advancement of the vaccine formulation into process development and manufacturing and the conduction of toxicity studies towards future phase I human clinical trials. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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Review

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19 pages, 1054 KiB

Open AccessReview

Leishmania Vesicle-Depleted Exoproteome: What, Why, and How?

by Sofia Esteves, Inês Costa, Sara Luelmo, Nuno Santarém and Anabela Cordeiro-da-Silva

Microorganisms 2022, 10(12), 2435; https://doi.org/10.3390/microorganisms10122435 - 08 Dec 2022

Cited by 4 | Viewed by 2100

Abstract

Leishmaniasis, a vector-borne parasitic protozoan disease, is among the most important neglected tropical diseases. In the absence of vaccines, disease management is challenging. The available chemotherapy is suboptimal, and there are growing concerns about the emergence of drug resistance. Thus, a better understanding of parasite biology is essential to generate new strategies for disease control. In this context, in vitro parasite exoproteome characterization enabled the identification of proteins involved in parasite survival, pathogenesis, and other biologically relevant processes. After 2005, with the availability of genomic information, these studies became increasingly feasible and revealed the true complexity of the parasite exoproteome. After the discovery of Leishmania extracellular vesicles (EVs), most exoproteome studies shifted to the characterization of EVs. The non-EV portion of the exoproteome, named the vesicle-depleted exoproteome (VDE), has been mostly ignored even if it accounts for a significant portion of the total exoproteome proteins. Herein, we summarize the importance of total exoproteome studies followed by a special emphasis on the available information and the biological relevance of the VDE. Finally, we report on how VDE can be studied and disclose how it might contribute to providing biologically relevant targets for diagnosis, drug, and vaccine development. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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21 pages, 871 KiB

Open AccessReview

Interspecies and Intrastrain Interplay among Leishmania spp. Parasites

by Bruna Dias das Chagas, Thaís Martins Pereira, Lilian Motta Cantanhêde, Gabriela Pereira da Silva, Mariana Côrtes Boité, Luiza de Oliveira Ramos Pereira and Elisa Cupolillo

Microorganisms 2022, 10(10), 1883; https://doi.org/10.3390/microorganisms10101883 - 21 Sep 2022

Cited by 4 | Viewed by 1973

Abstract

Leishmania parasites present astonishing adaptative abilities that represent a matter of life or death within disparate environments during the heteroxenous parasite life cycle. From an evolutionary perspective, organisms develop methods of overcoming such challenges. Strategies that extend beyond the genetic diversity have been discussed and include variability between parasite cells during the infections of their hosts. The occurrence of Leishmania subpopulation fluctuations with variable structural genomic contents demonstrates that a single strain might shelter the variability required to overcome inconsistent environments. Such intrastrain variability provides parasites with an extraordinary ability to adapt and thus survive and propagate. However, different perspectives on this evolution have been proposed. Strains or species living in the same environment can cooperate but also compete. These interactions might increase the replication rate of some parasites but cause the loss of more aggressive competitors for others. Adaptive responses to intra- and interspecific competition can evolve as a fixed strategy (replication is adapted to the average genetic complexity of infections) or an optional strategy (replication varies according to the genetic complexity of the current infection). This review highlights the complexity of interspecies and intrastrain interactions among Leishmania parasites as well as the different factors that influence this interplay. Full article

(This article belongs to the Special Issue Advances in Leishmania Research: From Basic Parasite Biology to Disease Control)

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