Early morning anopheline mosquito biting, a potential driver of malaria transmission in Busia County, western Kenya.
Anopheles
Human behavior
Insecticide Treated Nets (ITNs)
Malaria
Night-time observation
Journal
Malaria journal
ISSN: 1475-2875
Titre abrégé: Malar J
Pays: England
ID NLM: 101139802
Informations de publication
Date de publication:
04 Mar 2024
04 Mar 2024
Historique:
received:
13
10
2023
accepted:
27
02
2024
medline:
5
3
2024
pubmed:
5
3
2024
entrez:
4
3
2024
Statut:
epublish
Résumé
Insecticide-treated nets (ITNs) contributed significantly to the decline in malaria since 2000. Their protective efficacy depends not only on access, use, and net integrity, but also location of people within the home environment and mosquito biting profiles. Anopheline mosquito biting and human location data were integrated to identify potential gaps in protection and better understand malaria transmission dynamics in Busia County, western Kenya. Direct observation of human activities and human landing catches (HLC) were performed hourly between 1700 to 0700 h. Household members were recorded as home or away; and, if at home, as indoors/outdoors, awake/asleep, and under a net or not. Aggregated data was analysed by weighting hourly anopheline biting activity with human location. Standard indicators of human-vector interaction were calculated using a Microsoft Excel template. There was no significant difference between indoor and outdoor biting for Anopheles gambiae sensu lato (s.l.) (RR = 0.82; 95% CI 0.65-1.03); significantly fewer Anopheles funestus were captured outdoors than indoors (RR = 0.41; 95% CI 0.25-0.66). Biting peaked before dawn and extended into early morning hours when people began to awake and perform routine activities, between 0400-0700 h for An. gambiae and 0300-0700 h for An. funestus. The study population away from home peaked at 1700-1800 h (58%), gradually decreased and remained constant at 10% throughout the night, before rising again to 40% by 0600-0700 h. When accounting for resident location, nearly all bites within the peri-domestic space (defined as inside household structures and surrounding outdoor spaces) occurred indoors for unprotected people (98%). Using an ITN while sleeping was estimated to prevent 79% and 82% of bites for An. gambiae and An. funestus, respectively. For an ITN user, most remaining exposure to bites occurred indoors in the hours before bed and early morning. While use of an ITN was estimated to prevent most vector bites in this context, results suggest gaps in protection, particularly in the early hours of the morning when biting peaks and many people are awake and active. Assessment of additional human exposure points, including outside of the peri-domestic setting, are needed to guide supplementary interventions for transmission reduction.
Sections du résumé
BACKGROUND
BACKGROUND
Insecticide-treated nets (ITNs) contributed significantly to the decline in malaria since 2000. Their protective efficacy depends not only on access, use, and net integrity, but also location of people within the home environment and mosquito biting profiles. Anopheline mosquito biting and human location data were integrated to identify potential gaps in protection and better understand malaria transmission dynamics in Busia County, western Kenya.
METHODS
METHODS
Direct observation of human activities and human landing catches (HLC) were performed hourly between 1700 to 0700 h. Household members were recorded as home or away; and, if at home, as indoors/outdoors, awake/asleep, and under a net or not. Aggregated data was analysed by weighting hourly anopheline biting activity with human location. Standard indicators of human-vector interaction were calculated using a Microsoft Excel template.
RESULTS
RESULTS
There was no significant difference between indoor and outdoor biting for Anopheles gambiae sensu lato (s.l.) (RR = 0.82; 95% CI 0.65-1.03); significantly fewer Anopheles funestus were captured outdoors than indoors (RR = 0.41; 95% CI 0.25-0.66). Biting peaked before dawn and extended into early morning hours when people began to awake and perform routine activities, between 0400-0700 h for An. gambiae and 0300-0700 h for An. funestus. The study population away from home peaked at 1700-1800 h (58%), gradually decreased and remained constant at 10% throughout the night, before rising again to 40% by 0600-0700 h. When accounting for resident location, nearly all bites within the peri-domestic space (defined as inside household structures and surrounding outdoor spaces) occurred indoors for unprotected people (98%). Using an ITN while sleeping was estimated to prevent 79% and 82% of bites for An. gambiae and An. funestus, respectively. For an ITN user, most remaining exposure to bites occurred indoors in the hours before bed and early morning.
CONCLUSION
CONCLUSIONS
While use of an ITN was estimated to prevent most vector bites in this context, results suggest gaps in protection, particularly in the early hours of the morning when biting peaks and many people are awake and active. Assessment of additional human exposure points, including outside of the peri-domestic setting, are needed to guide supplementary interventions for transmission reduction.
Identifiants
pubmed: 38438933
doi: 10.1186/s12936-024-04893-3
pii: 10.1186/s12936-024-04893-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
66Subventions
Organisme : Unitaid
ID : 2018-29-UND
Informations de copyright
© 2024. The Author(s).
Références
Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.
pubmed: 26375008
pmcid: 4820050
doi: 10.1038/nature15535
WHO. Achieving and maintaining universal coverage with long-lasting insecticidal nets for malaria control. In: Global Malaria Programme. Geneva: World Health Organization 2017.
WHO. Global Technical Strategy for malaria 2016–2030. Geneva: World Health Organization; 2015.
Khanam F, Hossain MB, Chowdhury TR, Rahman MS, Kabir M, Naher S, et al. Exploring the gap between coverage, access, and utilization of long-lasting insecticide-treated nets (LLINs) among the households of malaria endemic districts in Bangladesh. Malar J. 2018;17:455.
pubmed: 30522487
pmcid: 6282300
doi: 10.1186/s12936-018-2610-0
Coalson JE, Santos EM, Little AC, Anderson EJ, Stroupe N, Agawo M, et al. Insufficient ratio of long-lasting insecticidal nets to household members limited universal usage in Western Kenya: a 2015 cross-sectional study. Am J Trop Med Hyg. 2020;102:1328–42.
pubmed: 32314696
pmcid: 7941599
doi: 10.4269/ajtmh.19-0119
Koenker H, Kilian A. Recalculating the net use gap: a multi-country comparison of ITN use versus ITN access. PLoS ONE. 2014;9: e97496.
pubmed: 24848768
pmcid: 4030003
doi: 10.1371/journal.pone.0097496
Bertozzi-Villa A, Bever CA, Koenker H, Weiss DJ, Vargas-Ruiz C, Nandi AK, et al. Maps and metrics of insecticide-treated net access, use, and nets-per-capita in Africa from 2000–2020. Nat Commun. 2021;12:3589.
pubmed: 34117240
pmcid: 8196080
doi: 10.1038/s41467-021-23707-7
Chandler JA, Highton RB, Hill MN. Mosquitoes of the Kano Plain, Kenya I Results of indoor collections in irrigated and nonirrigated areas using human bait and light traps. J Med Entomol. 1975;12:504–10.
pubmed: 4620
doi: 10.1093/jmedent/12.5.504
Gatton ML, Chitnis N, Churcher T, Donnelly MJ, Ghani AC, Godfray HC, et al. The importance of mosquito behavioural adaptations to malaria control in Africa. Evolution. 2013;67:1218–30.
pubmed: 23550770
pmcid: 3655544
doi: 10.1111/evo.12063
Sokhna C, Ndiath MO, Rogier C. The changes in mosquito vector behaviour and the emerging resistance to insecticides will challenge the decline of malaria. Clin Microbiol Infect. 2013;19:902–7.
pubmed: 23910459
doi: 10.1111/1469-0691.12314
Sangbakembi-Ngounou C, Costantini C, Longo-Pendy NM, Ngoagouni C, Akone-Ella O, Rahola N, et al. Diurnal biting of malaria mosquitoes in the Central African Republic indicates residual transmission may be “out of control.” Proc Natl Acad Sci USA. 2022;119: e2104282119.
pubmed: 35576470
pmcid: 9173762
doi: 10.1073/pnas.2104282119
Wamae PM, Githeko AK, Otieno GO, Kabiru EW, Duombia SO. Early biting of the Anopheles gambiae s.s. and its challenges to vector control using insecticide treated nets in western Kenya highlands. Acta Trop. 2015;150:136–42.
pubmed: 26209103
doi: 10.1016/j.actatropica.2015.07.008
Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ, et al. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc Natl Acad Sci USA. 2019;116:15086–95.
pubmed: 31285346
pmcid: 6660788
doi: 10.1073/pnas.1820646116
Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.
pubmed: 21736750
pmcid: 3146901
doi: 10.1186/1475-2875-10-184
Monroe A, Moore S, Okumu F, Kiware S, Lobo NF, Koenker H, et al. Methods and indicators for measuring patterns of human exposure to malaria vectors. Malar J. 2020;19:207.
pubmed: 32546166
pmcid: 7296719
doi: 10.1186/s12936-020-03271-z
Moiroux N, Damien GB, Egrot M, Djenontin A, Chandre F, Corbel V, et al. Human exposure to early morning Anopheles funestus biting behavior and personal protection provided by long-lasting insecticidal nets. PLoS ONE. 2014;9: e104967.
pubmed: 25115830
pmcid: 4130624
doi: 10.1371/journal.pone.0104967
Cooke MK, Kahindi SC, Oriango RM, Owaga C, Ayoma E, Mabuka D, et al. ‘A bite before bed’: exposure to malaria vectors outside the times of net use in the highlands of western Kenya. Malar J. 2015;14:259.
pubmed: 26109384
pmcid: 4479228
doi: 10.1186/s12936-015-0766-4
Ochomo EO, Gimnig JE, Bhattarai A, Samuels AM, Kariuki S, Okello G, et al. Evaluation of the protective efficacy of a spatial repellent to reduce malaria incidence in children in western Kenya compared to placebo: study protocol for a cluster-randomized double-blinded control trial (the AEGIS program). Trials. 2022;23:260.
pubmed: 35382858
pmcid: 8980512
doi: 10.1186/s13063-022-06196-x
Monroe A, Moore S, Koenker H, Lynch M, Ricotta E. Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature. Malar J. 2019;18:6.
pubmed: 30634963
pmcid: 6329148
doi: 10.1186/s12936-019-2638-9
Ochomo E, Bayoh NM, Kamau L, Atieli F, Vulule J, Ouma C, et al. Pyrethroid susceptibility of malaria vectors in four Districts of western Kenya. Parasit Vectors. 2014;7:310.
pubmed: 24996418
pmcid: 4094666
doi: 10.1186/1756-3305-7-310
Russell TL, Staunton K, Burkot TR. Standard Operating Procedure for performing human landing catch protocols. 2022. https://www.protocols.io/view/standard-operating-procedure-for-performing-human-cbnvsme6
Coetzee M. Key to the females of Afrotropical Anopheles mosquitoes (Diptera: Culicidae). Malar J. 2020;19:70.
pubmed: 32054502
pmcid: 7020601
doi: 10.1186/s12936-020-3144-9
MR4. Methods in Anopheles Research. CDC Atlanta, Gorgia, USA. 2015.
Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.
pubmed: 8214283
doi: 10.4269/ajtmh.1993.49.520
Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group. Am J Trop Med Hyg. 2002;66:804–11.
pubmed: 12224596
doi: 10.4269/ajtmh.2002.66.804
Edwards HM, Sriwichai P, Kirabittir K, Prachumsri J, Chavez IF, Hii J. Transmission risk beyond the village: entomological and human factors contributing to residual malaria transmission in an area approaching malaria elimination on the Thailand-Myanmar border. Malar J. 2019;18:221.
pubmed: 31262309
pmcid: 6604376
doi: 10.1186/s12936-019-2852-5
Monroe A, Msaky D, Kiware S, Tarimo BB, Moore S, Haji K, et al. Patterns of human exposure to malaria vectors in Zanzibar and implications for malaria elimination efforts. Malar J. 2020;19:212.
pubmed: 32571338
pmcid: 7310102
doi: 10.1186/s12936-020-03266-w
Fernandez Montoya L, Alafo C, Martí-Soler H, Máquina M, Comiche K, Cuamba I, et al. Overlaying human and mosquito behavioral data to estimate residual exposure to host-seeking mosquitoes and the protection of bednets in a malaria elimination setting where indoor residual spraying and nets were deployed together. PLoS ONE. 2022;17: e0270882.
pubmed: 36107865
pmcid: 9477321
doi: 10.1371/journal.pone.0270882
Huho B, Briet O, Seyoum A, Sikaala C, Bayoh N, Gimnig J, et al. Consistently high estimates for the proportion of human exposure to malaria vector populations occurring indoors in rural Africa. Int J Epidemiol. 2013;42:235–47.
pubmed: 23396849
pmcid: 3600624
doi: 10.1093/ije/dys214
Bayoh MN, Walker ED, Kosgei J, Ombok M, Olang GB, Githeko AK, et al. Persistently high estimates of late night, indoor exposure to malaria vectors despite high coverage of insecticide treated nets. Parasit Vectors. 2014;7:380.
pubmed: 25141761
doi: 10.1186/1756-3305-7-380
Rozi IE, Syahrani L, Permana DH, Asih PBS, Hidayati APN, Kosasih S, et al. Human behavior determinants of exposure to Anopheles vectors of malaria in Sumba. Indonesia PLoS One. 2022;17: e0276783.
pubmed: 36374859
doi: 10.1371/journal.pone.0276783
Aubourg MA, Al-Amin HM, Sunkara A, Chetan S, Monroe A, Phru CS, et al. Human behaviour directs household-level exposure to malaria vectors in Bandarban. Bangladesh Malar J. 2022;21:355.
pubmed: 36443751
doi: 10.1186/s12936-022-04375-4
Killeen GF, Kihonda J, Lyimo E, Oketch FR, Kotas ME, Mathenge E, et al. Quantifying behavioural interactions between humans and mosquitoes: evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006;6:161.
pubmed: 17096840
pmcid: 1657018
doi: 10.1186/1471-2334-6-161
Seyoum A, Sikaala CH, Chanda J, Chinula D, Ntamatungiro AJ, Hawela M, et al. Human exposure to anopheline mosquitoes occurs primarily indoors, even for users of insecticide-treated nets in Luangwa Valley, South-east Zambia. Parasit Vectors. 2012;5:101.
pubmed: 22647493
pmcid: 3432592
doi: 10.1186/1756-3305-5-101
Russell TL, Govella NJ, Azizi S, Drakeley CJ, Kachur SP, Killeen GF. Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania. Malar J. 2011;10:80.
pubmed: 21477321
pmcid: 3084176
doi: 10.1186/1475-2875-10-80
Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239.
pubmed: 27113244
pmcid: 4845310
doi: 10.1186/s12936-016-1286-6
Musiba RM, Tarimo BB, Monroe A, Msaky D, Ngowo H, Mihayo K, et al. Outdoor biting and pyrethroid resistance as potential drivers of persistent malaria transmission in Zanzibar. Malar J. 2022;21:172.
pubmed: 35672768
pmcid: 9171934
doi: 10.1186/s12936-022-04200-y
Abong’o B, Gimnig JE, Longman B, Odongo T, Wekesa C, Webwile A, et al. Comparison of four outdoor mosquito trapping methods as potential replacements for human landing catches in western Kenya. Parasit Vectors. 2021;14:320.
pubmed: 34118973
pmcid: 8196510
doi: 10.1186/s13071-021-04794-3
Abong’o B, Gimnig JE, Torr SJ, Longman B, Omoke D, Muchoki M, et al. 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. 2020;10:4518.
pubmed: 32161302
pmcid: 7066154
doi: 10.1038/s41598-020-61350-2
Soma DD, Zogo B, Taconet P, Somé A, Coulibaly S, Baba-Moussa L, et al. Quantifying and characterizing hourly human exposure to malaria vectors bites to address residual malaria transmission during dry and rainy seasons in rural Southwest Burkina Faso. BMC Public Health. 2021;21:251.
pubmed: 33516197
pmcid: 7847557
doi: 10.1186/s12889-021-10304-y
Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.
pubmed: 24678587
pmcid: 3973838
doi: 10.1186/1475-2875-13-125
Monroe A, Asamoah O, Lam Y, Koenker H, Psychas P, Lynch M, et al. Outdoor-sleeping and other night-time activities in northern Ghana: implications for residual transmission and malaria prevention. Malar J. 2015;14:35.
pubmed: 25627277
pmcid: 4320825
doi: 10.1186/s12936-015-0543-4
Monroe A, Mihayo K, Okumu F, Finda M, Moore S, Koenker H, et al. Human behaviour and residual malaria transmission in Zanzibar: findings from in-depth interviews and direct observation of community events. Malar J. 2019;18:220.
pubmed: 31262306
pmcid: 6604484
doi: 10.1186/s12936-019-2855-2
Monroe A, Harvey SA, Lam Y, Muhangi D, Loll D, Kabali AT, et al. “People will say that I am proud”: a qualitative study of barriers to bed net use away from home in four Ugandan districts. Malar J. 2014;3:82.
doi: 10.1186/1475-2875-13-82
Eisele TP, Kleinschmidt I, Sarrassat S, terKuile F, Miller J, Chanda J, et al. Attractive targeted sugar bait phase III trials in Kenya, Mali, and Zambia. Trials. 2022;23:640.
doi: 10.1186/s13063-022-06555-8
Achee NL, Bangs MJ, Farlow R, Killeen GF, Lindsay S, Logan JG, et al. Spatial repellents: from discovery and development to evidence-based validation. Malar J. 2012;11:164.
pubmed: 22583679
pmcid: 3453515
doi: 10.1186/1475-2875-11-164