Investigating the Association Between Household Exposure to Anopheles Stephensi and Malaria in Sudan and Ethiopia: A Case-control Study Protocol

Background: Endemic African malaria vectors are poorly adapted to typical urban ecologies. However, Anopheles stephensi, an urban malaria vector formerly confined to South Asia and the Persian Gulf, was recently detected in Africa and may change the epidemiology of malaria across the continent. Little is known about the public health implications of An. stephensi in Africa. This study is designed to assess the relative importance of household exposure to An. stephensi and endemic malaria vectors for malaria risk in urban Sudan and Ethiopia.

Methods: Case-control studies will be conducted in 3 urban settings (2 in Sudan, 1 in Ethiopia) to assess the association between presence of An. stephensi in and around households and malaria. Cases, defined as individuals positive for Plasmodium falciparum and/or P. vivax by microscopy/rapid diagnostic test (RDT), and controls, defined as age-matched individuals negative for P. falciparum and/or P. vivax by microscopy/RDT, will be recruited from public health facilities. Both household surveys and entomological surveillance for adult and immature mosquitoes will be conducted at participant homes within 48 hours of enrolment. Adult and immature mosquitoes will be identified by polymerase chain reaction (PCR). Conditional logistic regression will be used to estimate the association between presence of An. stephensi and malaria status, adjusted for co-occurrence of other malaria vectors and participant gender.

Conclusions: Findings from this study will provide evidence of the relative importance of An. stephensi for malaria burden in urban African settings, shedding light on the need for future intervention planning and policy development.

References

Chakraborty N, Fry K, Behl R, Longfield K . Simplified Asset Indices to Measure Wealth and Equity in Health Programs: A Reliability and Validity Analysis Using Survey Data From 16 Countries. Glob Health Sci Pract. 2016; 4(1):141-54. PMC: 4807755. DOI: 10.9745/GHSP-D-15-00384. View

Coetzee M . Key to the females of Afrotropical Anopheles mosquitoes (Diptera: Culicidae). Malar J. 2020; 19(1):70. PMC: 7020601. DOI: 10.1186/s12936-020-3144-9. View

Hume J, Tunnicliff M, Ranford-Cartwright L, Day K . Susceptibility of Anopheles gambiae and Anopheles stephensi to tropical isolates of Plasmodium falciparum. Malar J. 2007; 6:139. PMC: 2148056. DOI: 10.1186/1475-2875-6-139. View

Balkew M, Mumba P, Dengela D, Yohannes G, Getachew D, Yared S . Geographical distribution of Anopheles stephensi in eastern Ethiopia. Parasit Vectors. 2020; 13(1):35. PMC: 6971998. DOI: 10.1186/s13071-020-3904-y. View

Djadid N, Gholizadeh S, Aghajari M, Zehi A, Raeisi A, Zakeri S . Genetic analysis of rDNA-ITS2 and RAPD loci in field populations of the malaria vector, Anopheles stephensi (Diptera: Culicidae): implications for the control program in Iran. Acta Trop. 2005; 97(1):65-74. DOI: 10.1016/j.actatropica.2005.08.003. View

Donnelly M, McCall P, Lengeler C, Bates I, DAlessandro U, Barnish G . Malaria and urbanization in sub-Saharan Africa. Malar J. 2005; 4:12. PMC: 552321. DOI: 10.1186/1475-2875-4-12. View

Alemu A, Tsegaye W, Golassa L, Abebe G . Urban malaria and associated risk factors in Jimma town, south-west Ethiopia. Malar J. 2011; 10:173. PMC: 3128012. DOI: 10.1186/1475-2875-10-173. View

Balkew M, Mumba P, Yohannes G, Abiy E, Getachew D, Yared S . An update on the distribution, bionomics, and insecticide susceptibility of Anopheles stephensi in Ethiopia, 2018-2020. Malar J. 2021; 20(1):263. PMC: 8189708. DOI: 10.1186/s12936-021-03801-3. View

Noor A, Elmardi K, Abdelgader T, Patil A, Amine A, Bakhiet S . Malaria risk mapping for control in the republic of Sudan. Am J Trop Med Hyg. 2012; 87(6):1012-1021. PMC: 3516068. DOI: 10.4269/ajtmh.2012.12-0390. View

10.

Faulde M, Rueda L, Khaireh B . First record of the Asian malaria vector Anopheles stephensi and its possible role in the resurgence of malaria in Djibouti, Horn of Africa. Acta Trop. 2014; 139:39-43. DOI: 10.1016/j.actatropica.2014.06.016. View

11.

Abubakr M, Sami H, Mahdi I, Altahir O, AbdElbagi H, Mohamed N . The Phylodynamic and Spread of the Invasive Asian Malaria Vectors, , in Sudan. Biology (Basel). 2022; 11(3). PMC: 8945054. DOI: 10.3390/biology11030409. View

12.

Sinka M, Pironon S, Massey N, Longbottom J, Hemingway J, Moyes C . A new malaria vector in Africa: Predicting the expansion range of and identifying the urban populations at risk. Proc Natl Acad Sci U S A. 2020; 117(40):24900-24908. PMC: 7547157. DOI: 10.1073/pnas.2003976117. View

13.

Harris P, Taylor R, Thielke R, Payne J, Gonzalez N, Conde J . Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2008; 42(2):377-81. PMC: 2700030. DOI: 10.1016/j.jbi.2008.08.010. View

14.

Tadesse F, Ashine T, Teka H, Esayas E, Messenger L, Chali W . Anopheles stephensi Mosquitoes as Vectors of Plasmodium vivax and falciparum, Horn of Africa, 2019. Emerg Infect Dis. 2021; 27(2):603-607. PMC: 7853561. DOI: 10.3201/eid2702.200019. View

15.

Hay S, Guerra C, Tatem A, Atkinson P, Snow R . Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol. 2004; 3(1):81-90. PMC: 3130901. DOI: 10.1038/nrmicro1069. View

16.

Havryliuk T, Ferreira M . A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz. 2009; 104(1):67-73. DOI: 10.1590/s0074-02762009000100011. View

17.

Ahmed A, Irish S, Zohdy S, Yoshimizu M, Tadesse F . Strategies for conducting Anopheles stephensi surveys in non-endemic areas. Acta Trop. 2022; 236:106671. PMC: 11004664. DOI: 10.1016/j.actatropica.2022.106671. View

18.

Tadesse F, Fogarty A, Deressa W . Prevalence and associated risk factors of malaria among adults in East Shewa Zone of Oromia Regional State, Ethiopia: a cross-sectional study. BMC Public Health. 2017; 18(1):25. PMC: 5513396. DOI: 10.1186/s12889-017-4577-0. View

19.

Elagali A, Ahmed A, Makki N, Ismail H, Ajak M, Alene K . Spatiotemporal mapping of malaria incidence in Sudan using routine surveillance data. Sci Rep. 2022; 12(1):14114. PMC: 9387890. DOI: 10.1038/s41598-022-16706-1. View

20.

Ashine T, Eyasu A, Asmamaw Y, Simma E, Zemene E, Epstein A . Spatiotemporal distribution and bionomics of Anopheles stephensi in different eco-epidemiological settings in Ethiopia. Parasit Vectors. 2024; 17(1):166. PMC: 10983662. DOI: 10.1186/s13071-024-06243-3. View