Species composition of sand flies and bionomics of Phlebotomus papatasi and P. sergenti (Diptera: Psychodidae) in cutaneous leishmaniasis endemic foci, Morocco

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Abstract

Background

Cutaneous Leishmaniasis (CL) is one of the most neglected tropical diseases in Morocco. Leishmania major and L. tropica are the main culprits identified in all endemic foci across the country. These two etiological agents are transmitted by Phlebotomus papatasi and P. sergenti, the two most prevalent sand fly species in Morocco. Previous studies reflected gaps of knowledge regarding the environmental fingerprints that affect the distribution of these two potential vectors across Morocco.

Methods

The sand flies were collected from 48 districts across Morocco using sticky paper traps. Collected specimens were preserved in 70 % ethanol for further processing and identification. Male and female densities were calculated in each site to examine their relations to the environmental conditions across these sites. The study used 19 environmental variables including precipitation, aridity, elevation, soil variables and a composite representing maximum, minimum and mean of day- and night-time Land Surface Temperature (LST), and Normalized Difference Vegetation Index (NDVI).

Results

A total of 11,717 specimens were collected during this entomological survey. These specimens represented 11 species of two genera; Phlebotomus and Sergentomyia. Correlations of the sand fly densities with the environmental variables were estimated to identify the variables which influence the distribution of the two potential vectors, Phlebotomus papatasi and P. sergenti, associated with all CL endemic foci across the country. The density of P. papatasi was most affected by temperature changes. The study showed a significant positive correlation between the densities of both sexes of P. papatasi and night-time temperatures. Both P. papatasi and P. sergenti showed a negative correlation with aridity, but, such correlation was only significant in case of P. papatasi.

NDVI showed a positive correlation only with densities of P. sergenti, while, soil PH and soil water stress were negatively correlated with the densities of both males and females of only P. papatasi.

Conclusions

Our results identified the sand fly species across all CL endemic sites and underlined the influences of night-time temperature, soil water stress and NDVI as the most important variables affecting the sand fly distribution in all sampled sites. This preliminary study considered the importance of these covariates to anticipate the potential distribution of P. papatasi and P. sergenti in Morocco.

Electronic supplementary material

The online version of this article (doi:10.1186/s13071-016-1343-6) contains supplementary material, which is available to authorized users.

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Most cited references 45

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Sandflies of the Phlebotomus perniciosus complex: mitochondrial introgression and a new sibling species of P. longicuspis in the Moroccan Rif.

J Ready, J. Serrano, Manlio Márquez … (2004)

The bloodsucking adult females of Phlebotomus perniciosus Newstead and P. longicuspis Nitzulescu (Diptera: Psychodidae) are important vectors of the protozoan Leishmania infantum Nicolle (Kinetoplastida: Trypanosomatidae) in western Mediterranean countries. The species status of the two phlebotomine sandflies was assessed, along with the epidemiological implications. Individual sandflies from three Moroccan Rif populations were characterized morphologically, isoenzymatically (by the isoelectrofocusing of alleles at the polymorphic enzyme loci of HK, GPI and PGM), and by comparative DNA sequence analysis of a fragment of mitochondrial Cytochrome b (mtDNA). By reference to the character profiles of specimens from other locations, including southern Spain and the type-locality countries, the Moroccan flies were placed in three lineages: first, the lineage of P. perniciosus, which contained two mtDNA sublineages, one (pnt) widely distributed and associated with the morphology of the male types from Malta, and the other (pna) associated with a P. longicuspis-like male morphology; second, the lineage of P. longicuspis sensu stricto, including typical forms from Tunisia; and third, a new sibling species of P. longicuspis. The mtDNA sublineage (pnt) of typical P. perniciosus was also found in some P. longicuspis from Morocco, indicating interspecific hybridization. The typical race of P. perniciosus occurs in Italy as well as in Malta, Tunisia and Morocco. It is replaced in southern Spain by the Iberian race (with the pni mtDNA sublineage). The discovery of interspecific gene introgression and a new sibling species mean that previous records of the two morphospecies do not necessarily reflect their true vectorial roles or geographical and ecological distributions.

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[Human leishmaniases in Morocco: a nosogeographical diversity].

M Rhajaoui (2011)

Leishmaniases in Morocco are endemic diseases. Three forms of leishmaniasis are reported, visceral leishmaniasis, cutaneous leishmaniasis caused by Leishmania tropica and cutaneous lesions due to Leishmania major. Leishmania infantum, a common parasite inducing visceral leishmaniasis, was observed thereafter in cutaneous lesions. The first case of cutaneous leishmaniasis due to L. tropica was isolated since 1987. But, this parasite was shown to be more polymorphic with almost 8 zymodemes. However, these zymodemes are not all transmitted by Phlebotomus sergenti and not all isolated from human reservoir. Regarding the clinical aspect, cutaneous leishmaniasis with L. tropica is described as a single lesion starting as a nodule at the site of inoculation. A crust develops centrally which may fall away exposing an ulcer which heals gradually. The second cutaneous form is that caused by Leishmania major. It was known in villages located in the southern slopes of the Atlas Mountains. Clinically, the lesion is often severely inflamed and ulcerated and heals in 4-6 months. The epidemiologic cycle of this rural form, include Phlebotomus papatasi as the proven vector and a commensally rodent, Meriones shawi grandis as the reservoir. However, visceral leishmaniasis in Morocco has been known since 1921. It is especially located in the North. The responsible parasite is L. infantum MON 1. Two species of the sand fly are involved in the transmission of this form, P. ariasi and P. perniciosus. In infected man, the clinical signs are non-tender splenomegaly, with or without hepatomegaly, wasting and pallor of mucous membranes. Even though L. infantum MON1 is responsible of the disease, some canine cases were reported to be caused by Leishmania tropica. Copyright © 2009 Elsevier Masson SAS. All rights reserved.

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Detection and molecular typing of Leishmania tropica from Phlebotomus sergenti and lesions of cutaneous leishmaniasis in an emerging focus of Morocco

Malika Ajaoud, Nargys Es-sette, Salsabil Hamdi … (2013)

Background Cutaneous leishmaniasis is an infectious disease caused by flagellate protozoa of the genus Leishmania. In Morocco, anthroponotic cutaneous leishmaniasis due to Leishmania tropica is considered as a public health problem, but its epidemiology has not been fully elucidated. The main objective of this study was to detect Leishmania infection in the vector, Phlebotomus sergenti and in human skin samples, in the El Hanchane locality, an emerging focus of cutaneous leishmaniasis in central Morocco. Methods A total of 643 sand flies were collected using CDC miniature light traps and identified morphologically. Leishmania species were characterized by ITS1 PCR-RFLP and ITS1-5.8S rRNA gene nested-PCR of samples from 123 females of Phlebotomus sergenti and 7 cutaneous leishmaniasis patients. Results The sand flies collected consisted of 9 species, 7 of which belonged to the genus Phlebotomus and two to the genus Sergentomyia. Phlebotomus sergenti was the most predominant (76.67%). By ITS1 PCR-RFLP Leishmania tropica was found in three Phlebotomus sergenti females and four patients (4/7). Using nested PCR Leishmania tropica was identified in the same three Phlebotomus sergenti females and all the 7 patients. The sequencing of the nested PCR products recognized 7 haplotypes, of which 6 have never been described. Conclusions This is the first molecular detection and identification of Leishmania tropica in human skin samples and Phlebotomus sergenti in support of its vector status in El Hanchane. The finding of seven Leishmania tropica haplotypes underscores heterogeneity of this species at a high level in Morocco.

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Author and article information

Contributors

Samia Boussaa: samiaboussaa@gmail.com

Kholoud Kahime: kahimkholoud@gmail.com

Abdallah M. Samy: samy@sci.asu.edu.eg

Abdelkrim Ben Salem: bensalemk@gmail.com

Ali Boumezzough: boumezzough@uca.ma

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 2 February 2016

Publication date PMC-release: 2 February 2016

Publication date Collection: 2016

Volume: 9

Electronic Location Identifier: 60

Affiliations

[ ]Laboratory of Ecology and Environment (URAC 32, CNRST; ERACNERS 06), Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco

[ ]Institut Supérieur des Professions Infirmières et des Techniques de Santé (ISPITS), Ministry of Health, Marrakesh, Morocco

[ ]Entomology Department, Faculty of Science, Ain Shams University, Cairo, 11566 Egypt

[ ]Laboratory of Hydrobiology, Ecotoxicology and Sanitation (LHEA), Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco

Article

Publisher ID: 1343

DOI: 10.1186/s13071-016-1343-6

PMC ID: 4736259

PubMed ID: 26830689

SO-VID: 5cd6584b-9427-4a1b-8d85-822355382dd8

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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

Date received : 21 October 2015

Date accepted : 26 January 2016

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ScienceOpen disciplines: Parasitology

Keywords: phlebotomus papatasi,p. sergenti,temperature,soil,ndvi,environmental factors,cutaneous leishmaniasis,morocco

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ScienceOpen disciplines: Parasitology

Keywords: phlebotomus papatasi, p. sergenti, temperature, soil, ndvi, environmental factors, cutaneous leishmaniasis, morocco

Species composition of sand flies and bionomics of Phlebotomus papatasi and P. sergenti (Diptera: Psychodidae) in cutaneous leishmaniasis endemic foci, Morocco

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Abstract

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Malaria vaccine development

Most cited references 45

Sandflies of the Phlebotomus perniciosus complex: mitochondrial introgression and a new sibling species of P. longicuspis in the Moroccan Rif.

[Human leishmaniases in Morocco: a nosogeographical diversity].

Detection and molecular typing of Leishmania tropica from Phlebotomus sergenti and lesions of cutaneous leishmaniasis in an emerging focus of Morocco

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