Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia

Temesgen Ashine; Adane Eyasu; Yehenew Asmamaw; Eba Simma; Endalew Zemene; Adrienne Epstein; Rebecca Brown; Nigatu Negash; Abena Kochora; Alison Reynolds; Mikiyas Gebremichael Bulto; Temesgen Tafesse; Alemayehu Dagne; Biniyam Lukus; Endashaw Esayas; Sinknesh Wolde Behaksra; Kidist Woldekidan; Fikregabrail Aberra Kassa; Jimma Dinsa Deressa; Muluken Assefa; Dereje Dillu; Gudissa Assefa; Hiwot Solomon; Ahmed Zeynudin; Fekadu Massebo; Luigi Sedda; Martin Donnelly; Anne Wilson; David Weetman; Endalamaw Gadisa; Delenasaw Yewhalaw

doi:10.1186/s13071-024-06243-3

Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia

Temesgen Ashine, Adane Eyasu, Yehenew Asmamaw, Eba Simma, Endalew Zemene, Adrienne Epstein, Rebecca Brown, Nigatu Negash, Abena Kochora, Alison Reynolds, Mikiyas Gebremichael Bulto, Temesgen Tafesse, Alemayehu Dagne, Biniyam Lukus, Endashaw Esayas, Sinknesh Wolde Behaksra, Kidist Woldekidan, Fikregabrail Aberra Kassa, Jimma Dinsa Deressa, Muluken AssefaDereje Dillu, Gudissa Assefa, Hiwot Solomon, Ahmed Zeynudin, Fekadu Massebo, Luigi Sedda, Martin Donnelly, Anne Wilson, David Weetman, Endalamaw Gadisa, Delenasaw Yewhalaw

Vector Biology

Research output: Contribution to journal › Article › peer-review

18 Citations (Scopus)

Abstract

Background: Malaria is a major public health concern in Ethiopia, and its incidence could worsen with the spread of the invasive mosquito species Anopheles stephensi in the country. This study aimed to provide updates on the distribution of An. stephensi and likely household exposure in Ethiopia.

Methods: Entomological surveillance was performed in 26 urban settings in Ethiopia from 2021 to 2023. A kilometer-by-kilometer quadrant was established per town, and approximately 20 structures per quadrant were surveyed every 3 months. Additional extensive sampling was conducted in 50 randomly selected structures in four urban centers in 2022 and 2023 to assess households’ exposure to An. stephensi. Prokopack aspirators and CDC light traps were used to collect adult mosquitoes, and standard dippers were used to collect immature stages. The collected mosquitoes were identified to species level by morphological keys and molecular methods. PCR assays were used to assess Plasmodium infection and mosquito blood meal source.

Results: Catches of adult An. stephensi were generally low (mean: 0.15 per trap), with eight positive sites among the 26 surveyed. This mosquito species was reported for the first time in Assosa, western Ethiopia. Anopheles stephensi was the predominant species in four of the eight positive sites, accounting for 75–100% relative abundance of the adult Anopheles catches. Household-level exposure, defined as the percentage of households with a peridomestic presence of An. stephensi, ranged from 18% in Metehara to 30% in Danan. Anopheles arabiensis was the predominant species in 20 of the 26 sites, accounting for 42.9–100% of the Anopheles catches. Bovine blood index, ovine blood index and human blood index values were 69.2%, 32.3% and 24.6%, respectively, for An. stephensi, and 65.4%, 46.7% and 35.8%, respectively, for An. arabiensis. None of the 197 An. stephensi mosquitoes assayed tested positive for Plasmodium sporozoite, while of the 1434 An. arabiensis mosquitoes assayed, 62 were positive for Plasmodium (10 for P. falciparum and 52 for P. vivax).

Conclusions: This study shows that the geographical range of An. stephensi has expanded to western Ethiopia. Strongly zoophagic behavior coupled with low adult catches might explain the absence of Plasmodium infection. The level of household exposure to An. stephensi in this study varied across positive sites. Further research is needed to better understand the bionomics and contribution of An. stephensi to malaria transmission. Graphical Abstract:

Original language	English
Article number	166
Pages (from-to)	e166
Journal	Parasites and Vectors
Volume	17
Issue number	1
Early online date	31 Mar 2024
DOIs	https://doi.org/10.1186/s13071-024-06243-3
Publication status	Published - 31 Mar 2024

Keywords

Anopheles stephensi
Blood meal source
Ethiopia
Household’s exposure
Spatiotemporal distribution
Sporozoite rate

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1186/s13071-024-06243-3Licence: CC BY

13071 2024 Article 6243Final published version, 2.82 MBLicence: CC BY

Cite this

Ashine, T., Eyasu, A., Asmamaw, Y., Simma, E., Zemene, E., Epstein, A., Brown, R., Negash, N., Kochora, A., Reynolds, A., Bulto, M. G., Tafesse, T., Dagne, A., Lukus, B., Esayas, E., Behaksra, S. W., Woldekidan, K., Kassa, F. A., Deressa, J. D., ... Yewhalaw, D. (2024). Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia. Parasites and Vectors, 17(1), e166. Article 166. https://doi.org/10.1186/s13071-024-06243-3

@article{4bd20adc093846a3ba07f9917729f102,

title = "Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia",

abstract = "Background: Malaria is a major public health concern in Ethiopia, and its incidence could worsen with the spread of the invasive mosquito species Anopheles stephensi in the country. This study aimed to provide updates on the distribution of An. stephensi and likely household exposure in Ethiopia. Methods: Entomological surveillance was performed in 26 urban settings in Ethiopia from 2021 to 2023. A kilometer-by-kilometer quadrant was established per town, and approximately 20 structures per quadrant were surveyed every 3 months. Additional extensive sampling was conducted in 50 randomly selected structures in four urban centers in 2022 and 2023 to assess households{\textquoteright} exposure to An. stephensi. Prokopack aspirators and CDC light traps were used to collect adult mosquitoes, and standard dippers were used to collect immature stages. The collected mosquitoes were identified to species level by morphological keys and molecular methods. PCR assays were used to assess Plasmodium infection and mosquito blood meal source. Results: Catches of adult An. stephensi were generally low (mean: 0.15 per trap), with eight positive sites among the 26 surveyed. This mosquito species was reported for the first time in Assosa, western Ethiopia. Anopheles stephensi was the predominant species in four of the eight positive sites, accounting for 75–100\% relative abundance of the adult Anopheles catches. Household-level exposure, defined as the percentage of households with a peridomestic presence of An. stephensi, ranged from 18\% in Metehara to 30\% in Danan. Anopheles arabiensis was the predominant species in 20 of the 26 sites, accounting for 42.9–100\% of the Anopheles catches. Bovine blood index, ovine blood index and human blood index values were 69.2\%, 32.3\% and 24.6\%, respectively, for An. stephensi, and 65.4\%, 46.7\% and 35.8\%, respectively, for An. arabiensis. None of the 197 An. stephensi mosquitoes assayed tested positive for Plasmodium sporozoite, while of the 1434 An. arabiensis mosquitoes assayed, 62 were positive for Plasmodium (10 for P. falciparum and 52 for P. vivax). Conclusions: This study shows that the geographical range of An. stephensi has expanded to western Ethiopia. Strongly zoophagic behavior coupled with low adult catches might explain the absence of Plasmodium infection. The level of household exposure to An. stephensi in this study varied across positive sites. Further research is needed to better understand the bionomics and contribution of An. stephensi to malaria transmission. Graphical Abstract:",

keywords = "Anopheles stephensi, Blood meal source, Ethiopia, Household{\textquoteright}s exposure, Spatiotemporal distribution, Sporozoite rate",

author = "Temesgen Ashine and Adane Eyasu and Yehenew Asmamaw and Eba Simma and Endalew Zemene and Adrienne Epstein and Rebecca Brown and Nigatu Negash and Abena Kochora and Alison Reynolds and Bulto, \{Mikiyas Gebremichael\} and Temesgen Tafesse and Alemayehu Dagne and Biniyam Lukus and Endashaw Esayas and Behaksra, \{Sinknesh Wolde\} and Kidist Woldekidan and Kassa, \{Fikregabrail Aberra\} and Deressa, \{Jimma Dinsa\} and Muluken Assefa and Dereje Dillu and Gudissa Assefa and Hiwot Solomon and Ahmed Zeynudin and Fekadu Massebo and Luigi Sedda and Martin Donnelly and Anne Wilson and David Weetman and Endalamaw Gadisa and Delenasaw Yewhalaw",

year = "2024",

month = mar,

day = "31",

doi = "10.1186/s13071-024-06243-3",

language = "English",

volume = "17",

pages = "e166",

journal = "Parasites and Vectors",

issn = "1756-3305",

publisher = "BioMed Central Ltd",

number = "1",

}

Ashine, T, Eyasu, A, Asmamaw, Y, Simma, E, Zemene, E, Epstein, A, Brown, R, Negash, N, Kochora, A, Reynolds, A, Bulto, MG, Tafesse, T, Dagne, A, Lukus, B, Esayas, E, Behaksra, SW, Woldekidan, K, Kassa, FA, Deressa, JD, Assefa, M, Dillu, D, Assefa, G, Solomon, H, Zeynudin, A, Massebo, F, Sedda, L, Donnelly, M, Wilson, A, Weetman, D, Gadisa, E & Yewhalaw, D 2024, 'Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia', Parasites and Vectors, vol. 17, no. 1, 166, pp. e166. https://doi.org/10.1186/s13071-024-06243-3

TY - JOUR

T1 - Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia

AU - Ashine, Temesgen

AU - Eyasu, Adane

AU - Asmamaw, Yehenew

AU - Simma, Eba

AU - Zemene, Endalew

AU - Epstein, Adrienne

AU - Brown, Rebecca

AU - Negash, Nigatu

AU - Kochora, Abena

AU - Reynolds, Alison

AU - Bulto, Mikiyas Gebremichael

AU - Tafesse, Temesgen

AU - Dagne, Alemayehu

AU - Lukus, Biniyam

AU - Esayas, Endashaw

AU - Behaksra, Sinknesh Wolde

AU - Woldekidan, Kidist

AU - Kassa, Fikregabrail Aberra

AU - Deressa, Jimma Dinsa

AU - Assefa, Muluken

AU - Dillu, Dereje

AU - Assefa, Gudissa

AU - Solomon, Hiwot

AU - Zeynudin, Ahmed

AU - Massebo, Fekadu

AU - Sedda, Luigi

AU - Donnelly, Martin

AU - Wilson, Anne

AU - Weetman, David

AU - Gadisa, Endalamaw

AU - Yewhalaw, Delenasaw

PY - 2024/3/31

Y1 - 2024/3/31

N2 - Background: Malaria is a major public health concern in Ethiopia, and its incidence could worsen with the spread of the invasive mosquito species Anopheles stephensi in the country. This study aimed to provide updates on the distribution of An. stephensi and likely household exposure in Ethiopia. Methods: Entomological surveillance was performed in 26 urban settings in Ethiopia from 2021 to 2023. A kilometer-by-kilometer quadrant was established per town, and approximately 20 structures per quadrant were surveyed every 3 months. Additional extensive sampling was conducted in 50 randomly selected structures in four urban centers in 2022 and 2023 to assess households’ exposure to An. stephensi. Prokopack aspirators and CDC light traps were used to collect adult mosquitoes, and standard dippers were used to collect immature stages. The collected mosquitoes were identified to species level by morphological keys and molecular methods. PCR assays were used to assess Plasmodium infection and mosquito blood meal source. Results: Catches of adult An. stephensi were generally low (mean: 0.15 per trap), with eight positive sites among the 26 surveyed. This mosquito species was reported for the first time in Assosa, western Ethiopia. Anopheles stephensi was the predominant species in four of the eight positive sites, accounting for 75–100% relative abundance of the adult Anopheles catches. Household-level exposure, defined as the percentage of households with a peridomestic presence of An. stephensi, ranged from 18% in Metehara to 30% in Danan. Anopheles arabiensis was the predominant species in 20 of the 26 sites, accounting for 42.9–100% of the Anopheles catches. Bovine blood index, ovine blood index and human blood index values were 69.2%, 32.3% and 24.6%, respectively, for An. stephensi, and 65.4%, 46.7% and 35.8%, respectively, for An. arabiensis. None of the 197 An. stephensi mosquitoes assayed tested positive for Plasmodium sporozoite, while of the 1434 An. arabiensis mosquitoes assayed, 62 were positive for Plasmodium (10 for P. falciparum and 52 for P. vivax). Conclusions: This study shows that the geographical range of An. stephensi has expanded to western Ethiopia. Strongly zoophagic behavior coupled with low adult catches might explain the absence of Plasmodium infection. The level of household exposure to An. stephensi in this study varied across positive sites. Further research is needed to better understand the bionomics and contribution of An. stephensi to malaria transmission. Graphical Abstract:

AB - Background: Malaria is a major public health concern in Ethiopia, and its incidence could worsen with the spread of the invasive mosquito species Anopheles stephensi in the country. This study aimed to provide updates on the distribution of An. stephensi and likely household exposure in Ethiopia. Methods: Entomological surveillance was performed in 26 urban settings in Ethiopia from 2021 to 2023. A kilometer-by-kilometer quadrant was established per town, and approximately 20 structures per quadrant were surveyed every 3 months. Additional extensive sampling was conducted in 50 randomly selected structures in four urban centers in 2022 and 2023 to assess households’ exposure to An. stephensi. Prokopack aspirators and CDC light traps were used to collect adult mosquitoes, and standard dippers were used to collect immature stages. The collected mosquitoes were identified to species level by morphological keys and molecular methods. PCR assays were used to assess Plasmodium infection and mosquito blood meal source. Results: Catches of adult An. stephensi were generally low (mean: 0.15 per trap), with eight positive sites among the 26 surveyed. This mosquito species was reported for the first time in Assosa, western Ethiopia. Anopheles stephensi was the predominant species in four of the eight positive sites, accounting for 75–100% relative abundance of the adult Anopheles catches. Household-level exposure, defined as the percentage of households with a peridomestic presence of An. stephensi, ranged from 18% in Metehara to 30% in Danan. Anopheles arabiensis was the predominant species in 20 of the 26 sites, accounting for 42.9–100% of the Anopheles catches. Bovine blood index, ovine blood index and human blood index values were 69.2%, 32.3% and 24.6%, respectively, for An. stephensi, and 65.4%, 46.7% and 35.8%, respectively, for An. arabiensis. None of the 197 An. stephensi mosquitoes assayed tested positive for Plasmodium sporozoite, while of the 1434 An. arabiensis mosquitoes assayed, 62 were positive for Plasmodium (10 for P. falciparum and 52 for P. vivax). Conclusions: This study shows that the geographical range of An. stephensi has expanded to western Ethiopia. Strongly zoophagic behavior coupled with low adult catches might explain the absence of Plasmodium infection. The level of household exposure to An. stephensi in this study varied across positive sites. Further research is needed to better understand the bionomics and contribution of An. stephensi to malaria transmission. Graphical Abstract:

KW - Anopheles stephensi

KW - Blood meal source

KW - Ethiopia

KW - Household’s exposure

KW - Spatiotemporal distribution

KW - Sporozoite rate

U2 - 10.1186/s13071-024-06243-3

DO - 10.1186/s13071-024-06243-3

M3 - Article

SN - 1756-3305

VL - 17

SP - e166

JO - Parasites and Vectors

JF - Parasites and Vectors

IS - 1

M1 - 166

ER -

Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia

Abstract

Keywords

UN SDGs

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