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RefWorks
Reference Manager
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Zotero
EndNote
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Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP 2nd, Koech DK, 1988. Bloodmeal identification by direct enzyme-linked immunosorbent assay (Elisa), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 25: 9–16.
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11.
Scott JA, Brogdon WG, Collins FH, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520–529.
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12.
Hakizimana E, Karema C, Munyakanage D, Iranzi G, Githure J, Tongren JE, Takken W, Binagwaho A, Koenraadt CJM, 2016. Susceptibility of Anopheles gambiae to insecticides used for malaria vector control in Rwanda. Malar J 15: 582.
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World Health Organization, 2006. Guidelines for Testing Mosquito Adulticides for Indoor Residual Spraying and Treatment of Mosquito Nets. Geneva, Switzerland: WHO. Available at: https://apps.who.int/iris/bitstream/handle/10665/69296/WHO_CDS_NTD_WH?sequence=1.Accessed March 17, 2022.
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McCann RS, Ochomo E, Bayoh MN, Vulule JM, Hamel MJ, Gimnig JE, Hawley WA, Walker ED, 2014. Re-emergence of Anopheles funestus as a vector of Plasmodium falciparum in western Kenya after long-term implementation of Insecticide-Treated Bed Nets. Am J Trop Med Hyg 90: 597–604.
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Hay SI, Rogers DJ, Toomer JF, Snow RW, 2000. Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: Literature survey, internet access and review. Trans R Soc Trop Med Hyg 94: 113–127.
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Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, 2010. Anopheles gambiae: Historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62.
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Rwanda Biomedical Centre, 2016. Rwanda Malaria Program Mid Term Review – Final Report. Kigali, Rwanda: Ministry of Health, Republic of Rwanda.
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Kleinschmidt I, et al., 2018. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: A WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis 18: 640–649.
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Ochomo E, et al., 2017. Insecticide-treated nets and protection against insecticide-resistant malaria vectors in western Kenya. Emerg Infect Dis 23: 758–764.
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Lindblade KA, et al., 2015. A cohort study of the effectiveness of insecticide-treated bed nets to prevent malaria in an area of moderate pyrethroid resistance, Malawi. Malar J 14: 31.
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Grossman MK, Oliver SV, Brooke BD, Thomas MB, 2020. Use of alternative bioassays to explore the impact of pyrethroid resistance on LLIN efficacy. Parasit Vectors 13: 179.
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Gleave K, Lissenden N, Chaplin M, Choi L, Ranson H, 2021. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide‐treated nets to prevent malaria in Africa. Cochrane Database Syst Rev 5: CD012776.
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Mathias DK, et al., 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar J 10: 10.
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26.
Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF, 2011. A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg 85: 597–605.
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Anopheles gambiae Re-Emergence and Resurgent Malaria Transmission in Eastern Rwanda, 2010–2020
Ian Hennessee
i.p.hennessee@gmail.com
Ian Hennessee
Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia;
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Alphonse Mutabazi
Alphonse Mutabazi
Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda;
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Dunia Munyakanage
Dunia Munyakanage
Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda;
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Michee Kabera
Michee Kabera
Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda;
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Aimable Mbituyumuremyi
Aimable Mbituyumuremyi
Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda;
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Naomi Lucchi
Naomi Lucchi
U.S. President’s Malaria Initiative, U.S. Centers for Disease Control and Prevention, Kigali, Rwanda;
Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
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Miles A. Kirby
Miles A. Kirby
Department of Global Health and Population, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts;
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Lance A. Waller
Lance A. Waller
Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia;
Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia;
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Department of Biostatistics and Bioinformatics, Rollins School of Public Health, Emory University, Atlanta, Georgia;
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Thomas F. Clasen
Thomas F. Clasen
Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia;
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Uriel Kitron
Uriel Kitron
Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, Georgia;
Department of Environmental Sciences, Emory University, Atlanta, Georgia
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Department of Environmental Sciences, Emory University, Atlanta, Georgia
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Emmanuel Hakizimana
Emmanuel Hakizimana
Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda;
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ABSTRACT.
Rwanda achieved unprecedented malaria control gains from 2000 to 2010, but cases increased 20-fold between 2011 and 2017. Vector control challenges and environmental changes were noted as potential explanations, but no studies have investigated causes of the resurgence or identified which vector species drove transmission. We conducted a retrospective study in four sites in eastern Rwanda that conducted monthly entomological surveillance and outpatient malaria care. We compared sporozoite rates, human blood index (HBI), and relative abundance of the primary vectors, Anopheles gambiae and Anopheles arabiensis, from 2017 to 2020. We then modeled the effects of vector control interventions, insecticide resistance, and temperature changes on species composition and reported malaria incidence. Sporozoite rates were 28 times higher and HBI was four times higher in An. gambiae compared with An. arabiensis. Insecticide-treated bed nets, first distributed nationally in 2010, were associated with decreased An. gambiae relative abundance. However, increased pyrethroid resistance was associated with increased An. gambiae relative abundance and malaria incidence. Epidemic malaria peaks corresponded to periods of model-predicted An. gambiae re-emergence, and increased regional air temperatures during the period were further associated with increased malaria incidence. Indoor residual spraying (IRS), implemented with non-pyrethroid insecticides later in the period, was associated with 86% reductions in An. gambiae relative abundance and 75% reductions in malaria incidence. These findings suggest that increased pyrethroid resistance and the re-emergence of An. gambiae were closely linked to the malaria resurgence in eastern Rwanda. Non-pyrethroid IRS or other control measures that effectively target An. gambiae may help prevent future resurgences.
- Supplemental Materials (PDF 1564.4 KB)
Author Notes
Financial support: Research reported in this publication was supported by the
Disclosures: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the U.S. Centers for Disease Control and Prevention, the U.S. President Malaria Initiative, and the U.S. Agency for International Development.
Current contact information: Ian Hennessee, Lance A. Waller, Thomas F. Clasen, and Uriel Kitron, Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, GA, E-mails: i.p.hennessee@gmail.com, lwaller@emory.edu, thomas.f.clasen@emory.edu, and ukitron@emory.edu. Alphonse Mutabazi, Dunia Munyakanage, Michee Kabera, Aimable Mbituyumuremyi, and Emmanuel Hakizimana, Malaria and other Parasitic Diseases Division, Rwanda Biomedical Centre, Ministry of Health, Kigali, Rwanda, E-mails: alphonse.mutabazi@gmail.com, duniapopol@gmail.com, mickabera@yahoo.fr, aimable.mbituyumuremyi@gmail.com, and ehakizimana@gmail.com. Naomi Lucchi, U.S. President’s Malaria Initiative, U.S. Centers for Disease Control and Prevention, Kigali, Rwanda, and Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, GA, E-mail: frd9@cdc.gov. Miles A. Kirby, Department of Global Health and Population, Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, E-mail: miles.kirby@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Eckert E, et al., 2017. Impact evaluation of malaria control interventions on morbidity and all-cause child mortality in Rwanda, 2000–2010. Am J Trop Med Hyg 97: 99–110.
-
2.
President’s Malaria Initiative, 2019. Rwanda: Malaria Operational Plan FY 2019. Washington, DC: U.S. Agency for International Development.
-
3.
Malaria and Other Parasitic Diseases Division of the Rwanda Biomedical Center, Ministry of Health, and ICF, 2018. Rwanda Malaria Indicator Survey 2017 (MIS). Available at: https://dhsprogram.com/publications/publication-MIS30-MIS-Final-Reports.cfm. Accessed January 26, 2023.
-
4.
Karema C, Wen S, Sidibe A, Smith JL, Gosling R, Hakizimana E, Tanner M, Noor AM, Tatarsky A, 2020. History of malaria control in Rwanda: Implications for future elimination in Rwanda and other malaria-endemic countries. Malar J 19: 356.
-
5.
Hakizimana E, Karema C, Munyakanage D, Githure J, Mazarati JB, Tongren JE, Takken W, Binagwaho A, Koenraadt CJM, 2018. Spatio-temporal distribution of mosquitoes and risk of malaria infection in Rwanda. Acta Trop 182: 149–157.
-
6.
Konaté L, 2007. Rwanda Entomology Monitoring: Technical Report. Kigali, Rwanda: President’s Malaria Initiative.
-
7.
Howell PI, 2008. Summary of Anopheles gambiae Samples from Rwanda: Technical Report. Atlanta, GA: Centers for Disease Control and Prevention.
-
8.
World Health Organization, 2021. WHO Malaria Terminology. Geneva, Switzerland: WHO. Available at: https://www.who.int/publications/i/item/9789240038400. Accessed March 22, 2022.
-
9.
Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, Esser KM, Beaudoin RL, Andre RG, 1987. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 65: 39–45.
-
10.
Beier JC, Perkins PV, Wirtz RA, Koros J, Diggs D, Gargan TP 2nd, Koech DK, 1988. Bloodmeal identification by direct enzyme-linked immunosorbent assay (Elisa), tested on Anopheles (Diptera: Culicidae) in Kenya. J Med Entomol 25: 9–16.
-
11.
Scott JA, Brogdon WG, Collins FH, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520–529.
-
12.
Hakizimana E, Karema C, Munyakanage D, Iranzi G, Githure J, Tongren JE, Takken W, Binagwaho A, Koenraadt CJM, 2016. Susceptibility of Anopheles gambiae to insecticides used for malaria vector control in Rwanda. Malar J 15: 582.
-
13.
World Health Organization, 2006. Guidelines for Testing Mosquito Adulticides for Indoor Residual Spraying and Treatment of Mosquito Nets. Geneva, Switzerland: WHO. Available at: https://apps.who.int/iris/bitstream/handle/10665/69296/WHO_CDS_NTD_WH?sequence=1.Accessed March 17, 2022.
-
14.
World Health Organization, 2022. Manual for Monitoring Insecticide Resistance in Mosquito Vectors and Selecting Appropriate Interventions. Available at: https://www.who.int/publications-detail-redirect/9789240051089. Accessed May 8, 2024.
-
15.
Taylor KA, Koros JK, Nduati J, Copeland RS, Collins FH, Brandling-Bennett AD, 1990. Plasmodium falciparum infection rates in Anopheles gambiae, An. arabiensis, and An. funestus in western Kenya. Am J Trop Med Hyg 43: 124–129.
-
16.
McCann RS, Ochomo E, Bayoh MN, Vulule JM, Hamel MJ, Gimnig JE, Hawley WA, Walker ED, 2014. Re-emergence of Anopheles funestus as a vector of Plasmodium falciparum in western Kenya after long-term implementation of Insecticide-Treated Bed Nets. Am J Trop Med Hyg 90: 597–604.
-
17.
Hay SI, Rogers DJ, Toomer JF, Snow RW, 2000. Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: Literature survey, internet access and review. Trans R Soc Trop Med Hyg 94: 113–127.
-
18.
Bayoh MN, Mathias DK, Odiere MR, Mutuku FM, Kamau L, Gimnig JE, Vulule JM, Hawley WA, Hamel MJ, Walker ED, 2010. Anopheles gambiae: Historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malar J 9: 62.
-
19.
Rwanda Biomedical Centre, 2016. Rwanda Malaria Program Mid Term Review – Final Report. Kigali, Rwanda: Ministry of Health, Republic of Rwanda.
-
20.
Kleinschmidt I, et al., 2018. Implications of insecticide resistance for malaria vector control with long-lasting insecticidal nets: A WHO-coordinated, prospective, international, observational cohort study. Lancet Infect Dis 18: 640–649.
-
21.
Ochomo E, et al., 2017. Insecticide-treated nets and protection against insecticide-resistant malaria vectors in western Kenya. Emerg Infect Dis 23: 758–764.
-
22.
Lindblade KA, et al., 2015. A cohort study of the effectiveness of insecticide-treated bed nets to prevent malaria in an area of moderate pyrethroid resistance, Malawi. Malar J 14: 31.
-
23.
Grossman MK, Oliver SV, Brooke BD, Thomas MB, 2020. Use of alternative bioassays to explore the impact of pyrethroid resistance on LLIN efficacy. Parasit Vectors 13: 179.
-
24.
Gleave K, Lissenden N, Chaplin M, Choi L, Ranson H, 2021. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide‐treated nets to prevent malaria in Africa. Cochrane Database Syst Rev 5: CD012776.
-
25.
Mathias DK, et al., 2011. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in western Kenya. Malar J 10: 10.
-
26.
Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF, 2011. A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg 85: 597–605.
-
27.
Abong’o B, et al., 2020. Impact of indoor residual spraying with pirimiphos-methyl (Actellic 300CS) on entomological indicators of transmission and malaria case burden in Migori County, western Kenya. Sci Rep 10: 4518.
-
28.
Raouf S, et al., 2017. Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in an area of Uganda with previously high-transmission intensity. Clin Infect Dis 65: 453–460.
-
29.
Mawejje HD, et al., 2021. Impact of seasonality and malaria control interventions on Anopheles density and species composition from three areas of Uganda with differing malaria endemicity. Malar J 20: 138.
-
30.
Katureebe A, et al., 2016. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: A prospective observational study. PLoS Med 13: e1002167.
-
31.
Nuwa A, et al., 2022. District-led malaria surveillance and response as an effective way to manage malaria upsurges following the withdrawal of indoor residual spraying: A case study from Nwoya District, northern Uganda. Malar J 21: 55.
-
32.
Ngarukiyimana JP, Fu Y, Sindikubwabo C, Nkurunziza IF, Ogou FK, Vuguziga F, Ogwang BA, Yang Y, 2021. Climate Change in Rwanda: The Observed Changes in Daily Maximum and Minimum Surface Air Temperatures during 1961–2014. Available at: https://www.frontiersin.org/journals/earth-science/articles/10.3389/feart.2021.619512/full. Accessed March 22, 2022.
-
33.
Bouma MJ, Siraj AS, Rodo X, Pascual M, 2016. El Niño-based malaria epidemic warning for Oromia, Ethiopia, from August 2016 to July 2017. Trop Med Int Health 21: 1481–1488.
-
34.
Anyamba A, et al., 2019. Global disease outbreaks associated with the 2015–2016 El Niño event. Sci Rep 9: 1930.
-
35.
Mordecai EA, et al., 2013. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett 16: 22–30.
-
36.
Pascual M, Ahumada JA, Chaves LF, Rodo X, Bouma M, 2006. Malaria resurgence in the East African highlands: Temperature trends revisited. Proc Natl Acad Sci USA 103: 5829–5834.
-
37.
Siraj AS, Santos-Vega M, Bouma MJ, Yadeta D, Carrascal DR, Pascual M, 2014. Altitudinal changes in malaria incidence in highlands of Ethiopia and Colombia. Science 343: 1154–1158.
-
38.
WHO, 2019. World Malaria Report 2019. Geneva, Switzerland: World Health Organization, 2019. Available at: https://www.who.int/publications/i/item/world-malaria-report-2019. Accessed July 10, 2020.
-
39.
Bouma MJ, van der Kaay HJ, 1996. The El Niño Southern Oscillation and the historic malaria epidemics on the Indian subcontinent and Sri Lanka: An early warning system for future epidemics? Trop Med Int Health 1: 86–96.
-
40.
El Niño IRI, 2015. 2015 El Niño: Notes for the East African Malaria Community. New York, NY: Climate Information for Public Health Action: International Research Institute for Climate and Society. Available at: https://iri.columbia.edu/wp-content/uploads/2015/10/ElNino-Malaria-Oct-2015.pdf. Accessed November 11, 2021.
-
41.
Kilian AHD, Langi P, Talisuna A, Kabagambe G, 1999. Rainfall pattern, El Niño and malaria in Uganda. Trans R Soc Trop Med Hyg 93: 22–23.
-
42.
Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML, 1999. Highland malaria in Uganda: Prospective analysis of an epidemic associated with El Niño. Trans R Soc Trop Med Hyg 93: 480–487.
-
43.
Bayoh MN, et al., 2014. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors 7: 380.
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