Bionomic characterization of Anopheles mosquitoes in the Ethiopian highlands and lowlands.
Anopheles species
Ethiopia
Highland
Lowland
Malaria
Resident population
Seasonal migrant workers
Vector behaviors
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
16 Jul 2024
16 Jul 2024
Historique:
received:
31
03
2024
accepted:
26
06
2024
medline:
17
7
2024
pubmed:
17
7
2024
entrez:
16
7
2024
Statut:
epublish
Résumé
The protective effectiveness of vector control in malaria relies on how the implemented tools overlap with mosquito species-specific compositions and bionomic traits. In Ethiopia, targeted entomological data enabling strategic decision-making are lacking around high-risk migrant worker camps in the lowlands and resident communities in the highlands-resulting in suboptimal malaria control strategies for both populations. This study investigates spatial and temporal mosquito behavior, generating baseline evidence that will improve malaria control for both migrant workers in the lowlands and their home communities in the highlands. Hourly Centers for Disease Control and Prevention (CDC) light trap collections were performed indoors and outdoors during the peak (October to December 2022) and minor (March to May 2023) malaria transmission seasons. These seasons coincide with the post-long rain and post-short rain seasons, respectively. Eight resident households were sampled from each of four villages in the highlands and eight households/farm structures on and near farms in four villages in the lowlands. The sampling occurred between 18:00 and 06:00. Spatiotemporal vector behaviors and hourly indoor and outdoor mosquito capture rates, used as a proxy for human biting rates, were calculated for overall catches and for individual species. Adult mosquitoes were identified using morphological keys, and a subset of samples were confirmed to species by sequencing ribosomal DNA internal transcribed spacer region 2 (ITS2) and/or mitochondrial DNA cytochrome c oxidase subunit 1 (Cox1). In the highlands, 4697 Anopheles mosquitoes belonging to 13 morphologically identified species were collected. The predominant species of Anopheles identified in the highlands was An. gambiae sensu lato (s.l.) (n = 1970, 41.9%), followed by An. demeilloni (n = 1133, 24.1%) and An. cinereus (n = 520, 11.0%). In the lowland villages, 3220 mosquitoes belonging to 18 morphological species were collected. Anopheles gambiae s.l. (n = 1190, 36.9%), An. pretoriensis (n = 899, 27.9%), and An. demeilloni (n = 564, 17.5%) were the predominant species. A total of 20 species were identified molecularly, of which three could not be identified to species through comparison with published sequences. In highland villages, the indoor Anopheles mosquito capture rate was much greater than the outdoor rate. This trend reversed in the lowlands, where the rate of outdoor captures was greater than the indoor rate. In both highlands and lowlands, Anopheles mosquitoes showed early biting activities in the evening, which peaked between 18:00 and 21:00, for both indoor and outdoor locations. The high diversity of Anopheles vectors and their variable behaviors result in a dynamic and resilient transmission system impacting both exposure to infectious bites and intervention effectiveness. This creates gaps in protection allowing malaria transmission to persist. To achieve optimal control, one-size-fits-all strategies must be abandoned, and interventions should be tailored to the diverse spatiotemporal behaviors of different mosquito populations.
Sections du résumé
BACKGROUND
BACKGROUND
The protective effectiveness of vector control in malaria relies on how the implemented tools overlap with mosquito species-specific compositions and bionomic traits. In Ethiopia, targeted entomological data enabling strategic decision-making are lacking around high-risk migrant worker camps in the lowlands and resident communities in the highlands-resulting in suboptimal malaria control strategies for both populations. This study investigates spatial and temporal mosquito behavior, generating baseline evidence that will improve malaria control for both migrant workers in the lowlands and their home communities in the highlands.
METHODS
METHODS
Hourly Centers for Disease Control and Prevention (CDC) light trap collections were performed indoors and outdoors during the peak (October to December 2022) and minor (March to May 2023) malaria transmission seasons. These seasons coincide with the post-long rain and post-short rain seasons, respectively. Eight resident households were sampled from each of four villages in the highlands and eight households/farm structures on and near farms in four villages in the lowlands. The sampling occurred between 18:00 and 06:00. Spatiotemporal vector behaviors and hourly indoor and outdoor mosquito capture rates, used as a proxy for human biting rates, were calculated for overall catches and for individual species. Adult mosquitoes were identified using morphological keys, and a subset of samples were confirmed to species by sequencing ribosomal DNA internal transcribed spacer region 2 (ITS2) and/or mitochondrial DNA cytochrome c oxidase subunit 1 (Cox1).
RESULTS
RESULTS
In the highlands, 4697 Anopheles mosquitoes belonging to 13 morphologically identified species were collected. The predominant species of Anopheles identified in the highlands was An. gambiae sensu lato (s.l.) (n = 1970, 41.9%), followed by An. demeilloni (n = 1133, 24.1%) and An. cinereus (n = 520, 11.0%). In the lowland villages, 3220 mosquitoes belonging to 18 morphological species were collected. Anopheles gambiae s.l. (n = 1190, 36.9%), An. pretoriensis (n = 899, 27.9%), and An. demeilloni (n = 564, 17.5%) were the predominant species. A total of 20 species were identified molecularly, of which three could not be identified to species through comparison with published sequences. In highland villages, the indoor Anopheles mosquito capture rate was much greater than the outdoor rate. This trend reversed in the lowlands, where the rate of outdoor captures was greater than the indoor rate. In both highlands and lowlands, Anopheles mosquitoes showed early biting activities in the evening, which peaked between 18:00 and 21:00, for both indoor and outdoor locations.
CONCLUSIONS
CONCLUSIONS
The high diversity of Anopheles vectors and their variable behaviors result in a dynamic and resilient transmission system impacting both exposure to infectious bites and intervention effectiveness. This creates gaps in protection allowing malaria transmission to persist. To achieve optimal control, one-size-fits-all strategies must be abandoned, and interventions should be tailored to the diverse spatiotemporal behaviors of different mosquito populations.
Identifiants
pubmed: 39014474
doi: 10.1186/s13071-024-06378-3
pii: 10.1186/s13071-024-06378-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
306Informations de copyright
© 2024. The Author(s).
Références
Federal Ministry of Health (FMOH), Ethiopia. 2021. Ethiopia malaria elimination strategic plan: 2021–2025.
Graves PM, Richards FO, Ngondi J, Emerson PM, Shargie EB, Endeshaw T, et al. Individual, household and environmental risk factors for malaria infection in Amhara, Oromia and SNNP regions of Ethiopia. Trans R Soc Trop Med Hyg. 2009;103:1211–20.
doi: 10.1016/j.trstmh.2008.11.016
pubmed: 19144366
Federal Ministry of Health (FMOH), 2017 Ethiopia. National Malaria Strategic Plan: 2017–2020. Addis Ababa, Ethiopia: Disease Prevention and Control Directorate National Malaria Control and Elimination Program.
Esayas E, Tufa A, Massebo F, Ahemed A, Ibrahim I, Dillu D, et al. Malaria epidemiology and stratification of incidence in the malaria elimination setting in Harari Region. Eastern Ethiopia Infect Dis Poverty. 2020;9:160.
doi: 10.1186/s40249-020-00773-5
pubmed: 33222698
Ethiopian Public Health Institute (EPHI). Ethiopia National Malaria Indicator Survey 2015. Addis Ababa: Ethiopian Public Health Institute, Ministry of Health; 2016.
Tesfaye S, Belyhun Y, Teklu T, Mengesha T, Petros B. Malaria prevalence pattern observed in the highland fringe of Butajira, Southern Ethiopia: a longitudinal study from parasitological and entomological survey. Malar J. 2011;10:153.
doi: 10.1186/1475-2875-10-153
pubmed: 21649923
pmcid: 3141588
Daygena TY, Massebo F, Lindtjørn B. Variation in species composition and infection rates of Anopheles mosquitoes at different altitudinal transects, and the risk of malaria in the highland of Dirashe Woreda, south Ethiopia. Parasit Vectors. 2017;10:343.
doi: 10.1186/s13071-017-2288-0
pubmed: 28724450
pmcid: 5518156
Lemma W, Alemu K, Birhanie M, Worku L, Niedbalski J, McDowell MA, et al. Anopheles cinereus implicated as a vector of malaria transmission in the highlands of north-west Ethiopia. Parasit Vectors. 2019;12:557.
doi: 10.1186/s13071-019-3797-9
pubmed: 31767025
pmcid: 6878634
Dugassa S, Murphy M, Chibsa S, Tadesse Y, Yohannes G, Lorenz LM, et al. Malaria in migrant agricultural workers in western Ethiopia: entomological assessment of malaria transmission risk. Malar J. 2021;20:95.
doi: 10.1186/s12936-021-03633-1
pubmed: 33593385
pmcid: 7885338
Abeku TA. Malaria epidemics in Africa: prediction, detection and response. 2006; 20.
Lindsay SW, Martens W. Malaria in the African highlands: past, present and future. Bull World Health Organ. 1998;76:33–45.
pubmed: 9615495
pmcid: 2305628
Kiszewski A, Mellinger A, Spielman A, Malaney P, Sachs SE, Sachs J. A global index representing the stability of malaria transmission. Am J Trop Med Hyg. 2004;70:486–98.
doi: 10.4269/ajtmh.2004.70.486
pubmed: 15155980
Ranson H, Lissenden N. Insecticide resistance in African Anopheles mosquitoes: a worsening situation that needs urgent action to maintain malaria control. Trends Parasitol. 2016;32:187–96.
doi: 10.1016/j.pt.2015.11.010
pubmed: 26826784
Alemayehu E, Asale A, Eba K, Getahun K, Tushune K, Bryon A, et al. Mapping insecticide resistance and characterization of resistance mechanisms in Anopheles arabiensis (Diptera: Culicidae) in Ethiopia. Parasit Vectors. 2017;10:407.
doi: 10.1186/s13071-017-2342-y
pubmed: 28865490
pmcid: 5581456
Abose T. Reorientation and definition of the role of malaria vector control in Ethiopia. Geneva, Switzerland: World Health Organization; 1998.
Taye A, Hadis M, Adugna N, Tilahun D, Wirtz RA. Biting behavior and Plasmodium infection rates of Anopheles arabiensis from Sille. Ethiopia Acta Trop. 2006;97:50–4.
doi: 10.1016/j.actatropica.2005.08.002
pubmed: 16171769
Massebo F, Lindtjørn B. The effect of screening doors and windows on indoor density of Anopheles arabiensis in south-west Ethiopia: a randomized trial. Malaria J. 2013;12:319.
doi: 10.1186/1475-2875-12-319
Esayas E, Woyessa A, Massebo F. Malaria infection clustered into small residential areas in lowlands of southern Ethiopia. Parasit Epidemiol Cont. 2020;10:e00149.
doi: 10.1016/j.parepi.2020.e00149
Olbamo T, Esayas E, Gebre T, Massebo F. An evaluation of repellency and feeding inhibition of ethno-medicinal plants against major malaria vectors in southern Ethiopia. Parasit Vectors. 2021;14:190.
doi: 10.1186/s13071-021-04694-6
pubmed: 33827658
pmcid: 8025576
Balkew M, Mumba P, Yohannes G, Abiy E, Getachew D, Yared S, et al. An update on the distribution, bionomics, and insecticide susceptibility of Anopheles stephensi in Ethiopia, 2018–2020. Malar J. 2021;20:263.
doi: 10.1186/s12936-021-03801-3
pubmed: 34107943
pmcid: 8189708
Tadesse FG, Ashine T, Teka H, Esayas E, Messenger LA, Chali W, et al. Anopheles stephensi mosquitoes as vectors of Plasmodium vivax and falciparum, Horn of Africa, 2019. Emerg Infect Dis. 2021;27:603–7.
doi: 10.3201/eid2702.200019
pubmed: 33496217
pmcid: 7853561
Animut A, Lindtjørn B. Use of epidemiological and entomological tools in the control and elimination of malaria in Ethiopia. Malar J. 2018;17:26.
doi: 10.1186/s12936-018-2172-1
pubmed: 29329545
pmcid: 5767068
Ethiopia Central Statistical Agency (CSA), 2013. Population projections for Ethiopia 2007–2037.
Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara. Publ S Afr Inst Med Res. 1987;55:1–43.
Laurent BS, Cooke M, Krishnankutty SM, Asih P, Mueller JD, Kahindi S, et al. Molecular characterization reveals diverse and unknown malaria vectors in the western Kenyan highlands. Am J Trop Med Hyg. 2016;94:327–35.
doi: 10.4269/ajtmh.15-0562
Beebe NW, Saul A. Discrimination of all members of the Anopheles punctulatus complex by polymerase chain reaction-restriction fragment length polymorphism analysis. Am J Trop Med Hyg. 1995;1995:478–81.
doi: 10.4269/ajtmh.1995.53.478
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.
pubmed: 7881515
Ratnasingham S, Hebert PD. Bold: the barcode of life data system. Mol Ecol Notes. 2007;7:355–64.
doi: 10.1111/j.1471-8286.2007.01678.x
pubmed: 18784790
pmcid: 1890991
Harris PA, Taylor R, Minor BL, Elliott V, Fernandez M, O’Neal L, et al. The REDCap consortium: building an international community of software platform partners. J Biomed Inform. 2019;95:103208.
doi: 10.1016/j.jbi.2019.103208
pubmed: 31078660
pmcid: 7254481
Assa A, Eligo N, Massebo F. Anopheles mosquito diversity, entomological indicators of malaria transmission and challenges of morphological identification in southwestern Ethiopia. Trop Med Health. 2023;51:38.
doi: 10.1186/s41182-023-00529-5
pubmed: 37452392
pmcid: 10347854
Mwema T, Lukubwe O, Joseph R, Maliti D, Iitula I, Katokele S, et al. Human and vector behaviors determine exposure to Anopheles in Namibia. Parasit Vectors. 2022;15:436.
doi: 10.1186/s13071-022-05563-6
pubmed: 36397152
pmcid: 9673320
Paaijmans KP, Lobo NF. Gaps in protection: the actual challenge in malaria elimination. Malar J. 2023;22:46.
doi: 10.1186/s12936-023-04473-x
pubmed: 36747225
pmcid: 9902240
Mulambalah CS, Siamba DN, Ngeiywa MM, Vulule JM. Anopheles species diversity and breeding habitat distribution and the prospect for focused malaria control in the Western highlands of Kenya. Int J Trop Med. 2011;6:44–51.
doi: 10.3923/ijtmed.2011.44.51
Shililu J, Ghebremeskel T, Mengistu S, Fekadu H, Zerom M, Mbogo C, et al. Distribution of anopheline mosquitoes in Eritrea. Am J Trop Med Hyg. 2003;69:295–302.
doi: 10.4269/ajtmh.2003.69.295
pubmed: 14628947
Coetzee M, Craig M, Le Sueur D. Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today. 2000;16:74–7.
doi: 10.1016/S0169-4758(99)01563-X
pubmed: 10652493
Kibret S, Alemu Y, Boelee E, Tekie H, Alemu D, Petros B. The impact of a small-scale irrigation scheme on malaria transmission in Ziway area, central Ethiopia. Trop Med Int Health. 2010;15:41–50.
pubmed: 19917039
Kiware SS, Chitnis N, Tatarsky A, Wu S, Castellanos HM, Gosling R, et al. Attacking the mosquito on multiple fronts: insights from the vector control optimization model (VCOM) for malaria elimination. PLoS ONE. 2017;12:e0187680.
doi: 10.1371/journal.pone.0187680
pubmed: 29194440
pmcid: 5711017
Krafsur ES. Malaria transmission in Gambela, Illubabor Province. Ethiop Med J. 1971;9:75–94.
pubmed: 5149953
Kindu M, Aklilu E, Balkew M, Gebre-Michael T. Study on the species composition and ecology of anophelines in Addis Zemen, South Gondar. Ethiopia Parasit Vectors. 2018;11:215.
doi: 10.1186/s13071-018-2701-3
pubmed: 29587821
Carter TE, Yared S, Hansel S, Lopez K, Janies D. Sequence-based identification of Anopheles species in eastern Ethiopia. Malar J. 2019;18:135.
doi: 10.1186/s12936-019-2768-0
pubmed: 30992003
pmcid: 6469081
Lobo NF, Laurent BS, Sikaala CH, Hamainza B, Chanda J, Chinula D, et al. Unexpected diversity of Anopheles species in Eastern Zambia: implications for evaluating vector behavior and interventions using molecular tools. Sci Rep. 2015;5:17952.
doi: 10.1038/srep17952
pubmed: 26648001
pmcid: 4673690
Braack L, Hunt R, Koekemoer LL, Gericke A, Munhenga G, Haddow AD, et al. Biting behaviour of African malaria vectors: 1. where do the main vector species bite on the human body? Parasit Vectors. 2015;8:76.
doi: 10.1186/s13071-015-0677-9
pubmed: 25650005
pmcid: 4320538