A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system

Background: Visceral leishmaniasis (VL, or “kala-azar”) is a major cause of disability and death, especially in East Africa. Its vectors, sand flies (Diptera: Psychodidae: Phlebotominae), are poorly controlled and guarded against in these regions, owing in part to a lack of understanding about their...

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Main Authors: Solomon Yared, Araya Gebresilassie, Ibrahim Abbasi, Essayas Aklilu, Oscar D. Kirstein, Meshesha Balkew, Adam S. Brown, Ronald M. Clouse, Alon Warburg, Asrat Hailu, Teshome Gebre-Michael
Format: Article
Language:English
Published: Elsevier 2019-07-01
Series:Heliyon
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Online Access:http://www.sciencedirect.com/science/article/pii/S2405844019357925
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language English
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author Solomon Yared
Araya Gebresilassie
Ibrahim Abbasi
Essayas Aklilu
Oscar D. Kirstein
Meshesha Balkew
Adam S. Brown
Ronald M. Clouse
Alon Warburg
Asrat Hailu
Teshome Gebre-Michael
spellingShingle Solomon Yared
Araya Gebresilassie
Ibrahim Abbasi
Essayas Aklilu
Oscar D. Kirstein
Meshesha Balkew
Adam S. Brown
Ronald M. Clouse
Alon Warburg
Asrat Hailu
Teshome Gebre-Michael
A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
Heliyon
Agriculture
Ecology
Molecular biology
Zoology
author_facet Solomon Yared
Araya Gebresilassie
Ibrahim Abbasi
Essayas Aklilu
Oscar D. Kirstein
Meshesha Balkew
Adam S. Brown
Ronald M. Clouse
Alon Warburg
Asrat Hailu
Teshome Gebre-Michael
author_sort Solomon Yared
title A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
title_short A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
title_full A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
title_fullStr A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
title_full_unstemmed A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector system
title_sort molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern ethiopia reveals a complex host-vector system
publisher Elsevier
series Heliyon
issn 2405-8440
publishDate 2019-07-01
description Background: Visceral leishmaniasis (VL, or “kala-azar”) is a major cause of disability and death, especially in East Africa. Its vectors, sand flies (Diptera: Psychodidae: Phlebotominae), are poorly controlled and guarded against in these regions, owing in part to a lack of understanding about their feeding behavior. Methods: A total of 746 freshly fed female sand flies were collected in five population centers in Kafta Humera (northwestern Ethiopia), where VL is endemic. Flies were collected from habitats that ranged from inside houses to open fields, using light traps and sticky traps. Sources of sand fly blood meals were identified using enzyme-linked immunosorbent assays (ELISA) and DNA amplification with reverse-line blot analysis (PCR-RLB); 632 specimens were screened using ELISA, 408 of which had identifiable blood meals, and 114 were screened using PCR-RLB, 53 of which yielded identifications. Fly species determinations were based on morphology, and those specimens subjected to PCR-RLB were also screened for Leishmania parasites using conventional PCR to amplify the nuclear marker ITS1 (internal transcribed spacer 1) with Leishmania-specific primers. Results: More than three-fourths of all sand flies collected were Phlebotomus orientalis, and the remaining portion was comprised of nine other species. Nearly two-thirds of P. orientalis specimens were collected at village peripheries. The most common blood source for all flies was donkey (33.9% of all identifications), followed by cow (24.2%), human (17.6%), dog (11.8%), and goat or sheep (8.6%); mixtures of blood meals from different sources were found in 28.2% of all flies screened. Unidentified blood meals, presumably from wildlife, not domestic animals, were significantly higher in farm fields. Leishmania parasites were not detected in any of the 114 flies screened, not surprising given an expected infection rate of 1–5 out of 1,000. Meals that included a mixture of human and cow blood were significantly more frequent relative to all cow meals than human blood meals were to non-cow meals, suggesting a zoopotentiative interaction between cows and humans in this system. Conclusions: Habitat and host preferences of sand fly vectors in Kafta Humera confirmed the finding of previous reports that the main vector in the region, Phlebotomus orientalis, is a highly opportunistic feeder that prefers large animals and is most commonly found at village peripheries. These results were similar to those of a previous study conducted in a nearby region (Tahtay Adiabo), except for the role of cattle on the prevalence of human blood meals. Preliminary examinations of blood meal data from different settings point to the need for additional surveys and field experiments to understand the role of livestock on biting risks.
topic Agriculture
Ecology
Molecular biology
Zoology
url http://www.sciencedirect.com/science/article/pii/S2405844019357925
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spelling doaj-1a051951a3d24ffbb7540c136087bd872020-11-25T02:14:03ZengElsevierHeliyon2405-84402019-07-0157e02132A molecular analysis of sand fly blood meals in a visceral leishmaniasis endemic region of northwestern Ethiopia reveals a complex host-vector systemSolomon Yared0Araya Gebresilassie1Ibrahim Abbasi2Essayas Aklilu3Oscar D. Kirstein4Meshesha Balkew5Adam S. Brown6Ronald M. Clouse7Alon Warburg8Asrat Hailu9Teshome Gebre-Michael10Department of Biology, Jigjiga University, Jigjiga, EthiopiaDepartment of Zoological Sciences, Addis Ababa University, Addis Ababa, EthiopiaThe Kuvin Center for the Study of Infectious and Tropical Diseases, Institute for Medical Research, The Hebrew University, IsraelDepartment of Biology, Mada Walabu University, Bale-Robe, EthiopiaThe Kuvin Center for the Study of Infectious and Tropical Diseases, Institute for Medical Research, The Hebrew University, IsraelPresident's Malaria Initiative (PMI) Vector Link Project, EthiopiaHarvard University, Department of Biomedical Informatics, Boston, MA, United StatesAmerican Museum of Natural History, New York, NY, United States; Corresponding author.The Kuvin Center for the Study of Infectious and Tropical Diseases, Institute for Medical Research, The Hebrew University, IsraelDepartment of Microbiology, Immunology & Parasitology, School of Medicine; Addis Ababa University, Addis Ababa, EthiopiaAklilu Lemma Institute of Pathobiology, Addis Ababa University, Addis Ababa, EthiopiaBackground: Visceral leishmaniasis (VL, or “kala-azar”) is a major cause of disability and death, especially in East Africa. Its vectors, sand flies (Diptera: Psychodidae: Phlebotominae), are poorly controlled and guarded against in these regions, owing in part to a lack of understanding about their feeding behavior. Methods: A total of 746 freshly fed female sand flies were collected in five population centers in Kafta Humera (northwestern Ethiopia), where VL is endemic. Flies were collected from habitats that ranged from inside houses to open fields, using light traps and sticky traps. Sources of sand fly blood meals were identified using enzyme-linked immunosorbent assays (ELISA) and DNA amplification with reverse-line blot analysis (PCR-RLB); 632 specimens were screened using ELISA, 408 of which had identifiable blood meals, and 114 were screened using PCR-RLB, 53 of which yielded identifications. Fly species determinations were based on morphology, and those specimens subjected to PCR-RLB were also screened for Leishmania parasites using conventional PCR to amplify the nuclear marker ITS1 (internal transcribed spacer 1) with Leishmania-specific primers. Results: More than three-fourths of all sand flies collected were Phlebotomus orientalis, and the remaining portion was comprised of nine other species. Nearly two-thirds of P. orientalis specimens were collected at village peripheries. The most common blood source for all flies was donkey (33.9% of all identifications), followed by cow (24.2%), human (17.6%), dog (11.8%), and goat or sheep (8.6%); mixtures of blood meals from different sources were found in 28.2% of all flies screened. Unidentified blood meals, presumably from wildlife, not domestic animals, were significantly higher in farm fields. Leishmania parasites were not detected in any of the 114 flies screened, not surprising given an expected infection rate of 1–5 out of 1,000. Meals that included a mixture of human and cow blood were significantly more frequent relative to all cow meals than human blood meals were to non-cow meals, suggesting a zoopotentiative interaction between cows and humans in this system. Conclusions: Habitat and host preferences of sand fly vectors in Kafta Humera confirmed the finding of previous reports that the main vector in the region, Phlebotomus orientalis, is a highly opportunistic feeder that prefers large animals and is most commonly found at village peripheries. These results were similar to those of a previous study conducted in a nearby region (Tahtay Adiabo), except for the role of cattle on the prevalence of human blood meals. Preliminary examinations of blood meal data from different settings point to the need for additional surveys and field experiments to understand the role of livestock on biting risks.http://www.sciencedirect.com/science/article/pii/S2405844019357925AgricultureEcologyMolecular biologyZoology