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. 2023 May;29(5):945-955.
doi: 10.3201/eid2905.221657.

Leishmania donovani Transmission Cycle Associated with Human Infection, Phlebotomus alexandri Sand Flies, and Hare Blood Meals, Israel1

Leishmania donovani Transmission Cycle Associated with Human Infection, Phlebotomus alexandri Sand Flies, and Hare Blood Meals, Israel1

Liora Studentsky et al. Emerg Infect Dis. 2023 May.

Abstract

Cutaneous leishmaniasis caused by Leishmania major or L. tropica and visceral leishmaniasis caused by L. infantum have been reported in Israel. We collected Phlebotomus spp. sand flies in the Negev desert of southern Israel to identify circulating Leishmania spp. Of 22,636 trapped sand flies, 80% were P. alexandri. We sequenced Leishmania-specific internal transcribed spacer 1 fragments and K26 genes. Of 5,019 Phlebotomus female sand flies, 2.5% were Leishmania DNA-positive; 92% of infections were L. donovani. Phylogenetic analyses showed separate clustering of L. donovani and L. infantum. P. alexandri flies positive for L. donovani harbored blood meals from European hares. Leishmania DNA isolated from a patient with cutaneous leishmaniasis who lived in the survey area was identical to L. donovani from P. alexandri flies. We report circulation of L. donovani, a cause of visceral leishmaniasis, in southern Israel. Prompt diagnosis and Leishmania spp. identification are critical to prevent leishmaniasis progression.

Keywords: HRM; Israel; Leishmania donovani; Leishmania infantum; Phlebotomus alexandri; cutaneous leishmaniasis; high-resolution melting; parasites; sand fly; vector-borne infections; zoonoses.

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Figures

Figure 1
Figure 1
Locations of Phlebotomus spp. sand fly collection sites within the central Negev region of Israel in study of Leishmania donovani transmission cycle associated with human infection, Phlebotomus alexandri sand flies, and hare blood meals. We collected sand flies outdoors in August 2018, September 2019, and August 2020 by using modified traps from the US Centers for Disease Control and Prevention. The traps operated without light and were powered by 2 AA (1.2V) rechargeable batteries and baited with ≈1 kg dry ice. Traps were placed in an updraft vertical position overnight; openings were ≈10 cm above the ground, and collection cups hung above the motor and fan. Different colored circles indicate sites where specific Leishmania spp. infections were identified in trapped Phlebotomus sand flies. Empty circles indicate sites where sand flies were negative for Leishmania spp. Inset shows location of the survey area in Israel (red box).
Figure 3
Figure 3
Phylogenetic analysis of entire Leishmania internal transcribed spacer region in study of Leishmania donovani transmission cycle associated with human infection, Phlebotomus alexandri sand flies, and hare blood meals, Israel. Leishmania-specific internal transcribed spacer region (988 bp) was amplified by PCR from P. alexandri sand flies, pooled female Phlebotomus spp. flies, and patient samples and then sequenced. Tree was constructed by using by using the maximum-likelihood method and Tamura 3-parameter model of all relevant Leishmania spp. and Trypanosoma cruzi as an outgroup. Sand fly and clinical samples from this study (black triangles), L. infantum isolates from Israel (black circles), Leishmania international reference strains (empty circles), and available GenBank Leishmania sequences are shown. GenBank accession numbers, isolate source, and country of origin are shown for each sequence. Only bootstrap values >70% are shown next to branches. Not to scale.
Figure 2
Figure 2
Phylogenetic analysis of Leishmania internal transcribed spacer 1 rRNA fragments in study of Leishmania donovani transmission cycle associated with human infection, Phlebotomus alexandri sand flies, and hare blood meals, Israel. Leishmania-specific internal transcribed spacer 1 rRNA fragments (201 bp) were amplified by PCR from P. alexandri sand flies, pooled female Phlebotomus spp. flies, and patient samples and then sequenced. Tree was constructed by using the maximum-likelihood method and Tamura 3-parameter model, estimated by using the Aikaike information criterion (33). Dendogram includes sequences from L. donovani and L. infantum isolated from sand flies and clinical samples in this study compared with Leishmania spp. reference controls and GenBank sequences from Israel and other countries. Tree shows substantial separate clustering of L. infantum (boostrap 94%) and L. donovani (bootstrap 89%) sequences. Empty circles are Leishmania international reference strains, black triangles are the 10 sequences from our study deposited in GenBank, and black circles are additional L. infantum–positive sand flies samples from Israel. Available GenBank sequences for L. major, L. tropica, L. infantum, and L. donovani from Israel and other countries are also included. GenBank accession numbers, Leishmania spp., isolate source, and country are indicated. Only bootstrap values >70% are shown. Not to scale.
Figure 4
Figure 4
Phylogenetic analysis of Leishmania K26 gene in study of Leishmania donovani transmission cycle associated with human infection, Phlebotomus alexandri sand flies, and hare blood meals, Israel. Leishmania-specific K26 gene fragment (348 bp) was amplified by PCR from P. alexandri flies, pooled female Phlebotomus spp. flies, and patient samples and then sequenced. Tree was constructed by using the maximum-likelihood method and Hasegawa-Kishino-Yano model. K26 phylogenetic analysis shows separation between L. infantum and L. donovani. Sand fly and clinical samples from this study (black triangles), L. infantum isolates from Israel (black circles), Leishmania international reference strains (empty circles), and available GenBank Leishmania sequences are shown. GenBank accession number, isolate source, and country of origin are shown for each sequence. Only bootstrap values >70% are shown next to branches. Not to scale.

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