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. 2013;7(2):e2058.
doi: 10.1371/journal.pntd.0002058. Epub 2013 Feb 21.

A newly emerged cutaneous leishmaniasis focus in northern Israel and two new reservoir hosts of Leishmania major

Affiliations

A newly emerged cutaneous leishmaniasis focus in northern Israel and two new reservoir hosts of Leishmania major

Roy Faiman et al. PLoS Negl Trop Dis. 2013.

Abstract

In 2006/7, 18 cases of cutaneous leishmaniasis (CL) were reported for the first time from Sde Eliyahu (pop. 650), a village in the Beit She'an valley of Israel. Between 2007-2011, a further 88 CL cases were diagnosed bringing the total to 106 (16.3% of the population of Sde Eliyahu). The majority of cases resided in the south-western part of the village along the perimeter fence. The causative parasite was identified as Leishmania major Yakimoff & Schokhor, 1914 (Kinetoplastida: Trypanosomatidae). Phlebotomus papatasi (Scopoli), 1786 (Diptera: Psychodidae) was found to be the most abundant phlebotomine species comprising 97% of the sand flies trapped inside the village, and an average of 7.9% of the females were positive for Leishmania ITS1 DNA. Parasite isolates from CL cases and a sand fly were characterized using several methods and shown to be L. major. During a comprehensive survey of rodents 164 Levant voles Microtus guentheri Danford & Alston, 1880 (Rodentia: Cricetidae) were captured in alfalfa fields bordering the village. Of these 27 (16.5%) tested positive for Leishmania ITS1 DNA and shown to be L. major by reverse line blotting. A very high percentage (58.3%-21/36) of Tristram's jirds Meriones tristrami Thomas, 1892 (Rodentia: Muridae), found further away from the village also tested positive for ITS1 by PCR. Isolates of L. major were successfully cultured from the ear of a wild jird found positive by ITS1 PCR. Although none of the wild PCR-positive voles exhibited external pathology, laboratory-reared voles that were infected by intradermal L. major inoculation, developed patent lesions and sand flies became infected by feeding on the ears of these laboratory-infected voles. This is the first report implicating M. guentheri and M. tristrami as reservoirs of Leishmania. The widespread co-distribution of M. guentheri and P. papatasi, suggests a significant threat from the spread of CL caused by L. major in the Middle East, central Asia and southern Europe.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Annotated map of Sde Eliyahu and vicinity showing inhabited areas of the Kibbutz and the surrounding agricultural areas.
Houses where CL cases reside are marked with colored squares. The number of cases appears in each square and a darker color denotes more cases. The approximate location of different cultivars is marked and type of cultivar noted. The letter P in a red star denotes alfalfa fields where voles were captured by plowing, while a blue circle containing a W denotes the approximate location where voles were captured by flooding.
Figure 2
Figure 2. ITS1 PCR gel electrophoresis of DNA from lesion biopsies of ten cases of CL from Sde Eliyahu.
Top panel 300 bp, Leishmania ITS1 PCR product. Bottom panel shows the HAEIII restriction fragments of the ITS1 PCR product. Note the double-bands, identical to the pattern of L. major and very different from the L. tropica control.
Figure 3
Figure 3. The species composition of phlebotomine sand flies captured using CO2 baited traps.
A – Sample of sand flies trapped near the houses (n = 385) comprising 97.5% P. papatasi. B – Sample of sand flies trapped in an alfalfa field (n = 250) 1 km south of Kibbutz fence.
Figure 4
Figure 4. Detection and analyses of natural Leishmania infections in wild-caught voles.
Top Panel: Detection of Leishmania DNA by ITS1 PCR. Bottom Panel: Identification of PCR products by reverse-line blotting. PCR-positive samples (1,2,3 & 8) were identified as L. major.
Figure 5
Figure 5. Artificial L. major infections in voles.
(A) Leishmania-specific ITS1 PCR products (300 bp) in three voles, three weeks post-inoculation. Lanes 1,4,7 – ears. Lanes 2,5,8 – hind foot pads. Lanes 3,6,9 – snout. Biopsies were taken weekly after inoculation of 105 late log -phase L. major promastigotes in each inoculation site. −Ve – negative control without DNA, +Ve – positive control containing L. major DNA, mk – marker reference ladder. (B) Micrograph of tissue smear showing amastigotes-laden macrophages from the ear of a vole, six weeks P.I. (C) Blood smear showing free amastigotes. Peripheral blood from the hind foot pad of an infected vole seven weeks P.I. Scale bars = 10 μm.
Figure 6
Figure 6. Pathogenesis of artificial L. major infections in voles' ears and hind foot-pads.
Before infection (A, B), and 11 weeks post-infection with 105 late log-phase L. major promastigotes (C, D). Infected ears (C) typically swell, depilate and ulcerate. Infected hind foot pads (D) were nodulated, ulcerated, became erythematous and edematous.

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