Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 https://doi.org/10.1186/s13071‑022‑05179‑w Parasites & Vectors RESEARCH Open Access Spatiotemporal distribution and insecticide resistance status of Aedes aegypti in Ghana Christopher M. Owusu‑Asenso1, Julius A. A. Mingle1, David Weetman2 and Yaw A. Afrane1* Abstract Background: Vector control is the main intervention used to control arboviral diseases transmitted by Aedes mos‑ quitoes because there are no effective vaccines or treatments for most of them. Control of Aedes mosquitoes relies heavily on the use of insecticides, the effectiveness of which may be impacted by resistance. In addition, rational insecticide application requires detailed knowledge of vector distribution, dynamics, resting, and feeding behaviours, which are poorly understood for Aedes mosquitoes in Africa. This study investigated the spatiotemporal distribution and insecticide resistance status of Aedes aegypti across ecological extremes of Ghana. Methods: Immature mosquitoes were sampled from containers in and around human dwellings at seven study sites in urban, suburban, and rural areas of Ghana. Adult Aedes mosquitoes were sampled indoors and outdoors using Biogents BG‑Sentinel 2 mosquito traps, human landing catches, and Prokopack aspiration. Distributions of immature and adult Aedes mosquitoes were determined indoors and outdoors during dry and rainy seasons at all sites. The phenotypic resistance status of Aedes mosquitoes to insecticides was determined using World Health Organization susceptibility bioassays. The host blood meal source was determined by polymerase chain reaction. Results: A total of 16,711 immature Aedes were sampled, with over 70% found in car tyres. Significantly more breed‑ ing containers had Aedes immatures during the rainy season (11,856; 70.95%) compared to the dry season (4855; 29.05%). A total of 1895 adult Aedes mosquitos were collected, including Aedes aegypti (97.8%), Aedes africanus (2.1%) and Aedes luteocephalus (0.1%). Indoor sampling of adult Aedes yielded a total of 381 (20.1%) and outdoor sampling a total of 1514 (79.9%) mosquitoes (z = − 5.427, P = 0.0000) over the entire sampling period. Aedes aegypti populations were resistant to dichlorodiphenyltrichloroethane at all study sites. Vectors showed suspected resistance to bendio‑ carb (96–97%), permethrin (90–96%) and deltamethrin (91–96%), and were susceptible to the organophosphate for all study sites. Blood meal analysis showed that the Aedes mosquitoes were mostly anthropophilic, with a human blood index of 0.9 (i.e. humans, 90%; human and dog, 5%; dog and cow, 5%). Conclusions: Aedes mosquitoes were found at high densities in all ecological zones of Ghana. Resistance of Aedes spp. to pyrethroids and carbamates may limit the efficacy of vector control programmes and thus requires careful monitoring. Keywords: Aedes aegypti, Insecticide resistance, Human blood index, Seasons, Ghana Background Aedes aegypti and Aedes albopictus are the most impor- tant vectors of several arboviruses, notably yellow fever, dengue, chikungunya, and Zika virus [1]. The importance *Correspondence: yafrane@ug.edu.gh 1 of Aedes mosquitoes in sub-Saharan Africa has increased Department of Medical Microbiology, University of Ghana Medical School, University of Ghana, Korle‑Bu, Accra, Ghana recently because of outbreaks of arboviral diseases in Full list of author information is available at the end of the article multiple countries there [2]. In West Africa, within the © The Author(s) 2022. 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The Creative Commons Public Domain Dedication waiver (http:// creati veco mmons. org/ publi cdoma in/z ero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 2 of 14 last 5 years, there have been outbreaks of dengue in Bur- larvae, the degree of sunlight exposure [40], and con- kina Faso [3–5], Cote d’Ivoire [6, 7], and Senegal [8], yel- tainer coverings [41]. The adaptation of these vectors to low fever in Cote d’Ivoire [9–11] and Nigeria [12–16], urban domestic habitats has led to their exploitation of a and recent confirmed cases of dengue and outbreaks of range of artificial containers and their capacity to exploit yellow fever in Ghana [17–20]. Therefore, the risk of den- potential breeding water situated indoors or outdoors gue, yellow fever and chikungunya outbreaks in Ghana [42, 43]. appears to be high. Currently, and despite frequent concerns regarding the Aedes aegypti are highly anthropophilic and, through- efficacy of the methods used for their deployment [44], out most of the world, typically endophilic [21]. Imma- insecticidal interventions are the main tool used to con- ture stages develop preferentially in artificial containers, trol Aedes-borne arboviral infections, since vaccines for usually in close proximity to humans [22–25]. In sub- these are either unavailable, ineffective, or in limited sup- Saharan Africa, two morphological subspecies (ecotypes) ply [45–47]. To ensure that efficacy is maximised, correct have been acknowledged: domestic Aedes aegypti aegypti insecticide choice is crucial, and requires surveillance and sylvan Aedes aegypti formosus. The presence/absence to determine the susceptibility of target populations, of white abdominal scale patterns [26] is used to differen- alongside locating the adults and immatures that are to tiate the ecotypes, but at present, clear genetic bounda- be targeted [48]. Sustained effectiveness must also be ries appear to be absent, probably as a result of recent and considered: geographical variation in susceptibility may historical gene flow [27, 28]. Aedes aegypti formosus more rapidly lead to the spread of insecticide resistance and frequently breed away from domestic environments, and require revision regarding the most suitable insecticide feed readily on animals (zoophagy), so are less likely to for use. be a threat to humans in the urban environments where Another important parameter when considering how Aedes aegypti aegypti populations thrive [29]. However, to target vector control, especially for insecticidal spray urbanisation of the sylvatic environment could lead to deployment, is whether mosquitoes tend to rest indoors contact between Ae. aegypti formosus and humans, and (endophily) or outdoors (exophily) after blood-feeding this typically sylvatic species might adapt to new urban [49]. Insecticide-based intervention directed at the adult environments and hosts; it is also probable that intro- resting population is a relevant approach for Aedes con- gression through hybridization of urban and sylvatic sub- trol and disease prevention. Targeted indoor residual species of Ae. aegypti may lead to variation, potentially spraying on Aedes resting locations can provide a sig- increasing the role of Ae. aegypti formosus as vectors [28, nificant protective effect against arboviral transmission, 30]. The consistency of bionomic traits across ecozones and this method also has the potential to control pyre- remains poorly investigated. However, measures of abun- throid-resistant Aedes mosquitoes, as other classes of dance and distribution of Aedes would give more reliable insecticides (non-pyrethroids) are available for residual insights for both risk and mitigation strategies for infesta- application [50]. tions [31]. Several species of Aedes, including Aedes afri- This study aimed to characterize the breeding habitats, canus, readily feed on animals (both domestic and wild), seasonal abundance, and resting behaviour of Ae. aegypti, as well as humans, hence their potential importance as and their insecticide susceptibility, in rural, suburban, bridge vectors and for zoonotic transmission [32]. Iden- and urban sites in different ecological zones of Ghana. tification of the source of vector blood meals is critical to In addition to identifying targets and options for control, understanding the degree of human–vector interaction the results will also aid the development of a surveillance (i.e. anthropophily) [33, 34], which is a crucial parameter system for Aedes as vectors of arboviruses for the plan- in the estimation of the capacity of a vector to transmit a ning of disease control in Ghana [51, 52]. disease [35]. Seasonal variations in population density are expected Methods for Aedes, with lower abundances in dry seasons, rising Study sites with increasing temperatures, and potentially greater This study was carried out in seven sites comprising breeding site availability in the rainy season [36–38]. rural, suburban, and urban locations within the three However, human activities involving water storage and major ecological zones of Ghana, i.e. coastal savannah, the disposal of potential water-holding containers greatly forest, and Sahel savannah, across wet and dry seasons, influence the breeding of Aedes in individual households between May 2017 and May 2018. The selection of the and may lead to the provision of breeding sites year- study sites was based on both ecological zone and pop- round [39]. Key factors that may influence Aedes produc- ulation (urban, suburban, and rural), since variations in tivity in different container types include the frequency species, abundance, and susceptibility status of Aedes of water replenishment, the availability of food for the mosquitoes could be influenced by these parameters. O wusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 3 of 14 Residents in the rural study sites store water for domes- 5°33′0″N, 0°12′0″W), the capital of Ghana and its most tic use in diverse containers because the water supply populous city; and Tema (urban site; 5°40′0″N, 0°0′0″E), system is unreliable. Water supply in the rural study sites a port city where the importation of tyres from Asia is mainly from harvested rainwater, wells, and boreholes, and the Americas might facilitate the invasion of Aedes and these also supplement the irregular piped water genotypes or species previously unknown in Ghana. The supply system characteristic of our urban and suburban coastal savannah has a tropical savannah climate, with an study sites. Furthermore, it is known that Ae. aegypti is annual mean temperature of 26.5 °C and average annual adapted to urban settings while Ae. albopictus and other precipitation of 787 mm (Table 1). zoonotic species are found in the sylvatic zone. One of The urban site within the forest zone was Konongo the sites has a port where car tyres are imported, thus (06°37′00″N, 001°13′00″ W), a town located in Asante- may be a channel for the importation of species of Aedes Akim central district in the middle of Ghana. In the forest from the Americas previously unknown in Ghana. The zone, there is a high possibility that sylvan Aedes mosqui- sample sites are shown in Fig. 1. toes, which can serve as bridge vectors, might be present. In the coastal savannah zone of southern Ghana The forest zone has a tropical rainforest climate, with an the study sites were as follows: Ada Foah (suburban annual average temperature of 26.4  °C and annual aver- site; 5°47′N, 0°38′E), a tourist town; Accra (urban site; age precipitation of 1399.5 mm (Table 1). Fig. 1 Map of Ghana showing the study sites Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 4 of 14 Table 1 Study site locations Population Major ecological zones of Ghana Costal savannah Forest zone Sahel savannah Urban Accra (5°33′0″N, 0°12′0″W) Konongo (06°37′00″N, 01°13′00″W) Navrongo (10°53′5″N, 01°05′25″W) Tema (5°40′0″N, 0°0′0″E) Suburban Ada Foah (5°47’N, 0°38’E) Paga (10°59′32″N, 01°06′48″W) Rural Larabanga (9°5′0″N, 1°49′0″W) The sites in the Sahel savannah ecological zone were using pipettes and ladles [39, 55], counted, and recorded Larabanga, Navrongo, and Paga. Larabanga (rural site; on field data forms. Water from large containers was 9°5′0″N, 1°49′0″W) is a village situated close to Mole first sieved and larval samples placed in a white plastic national park, which harbours monkeys that could serve tray with some of the water in which they were pipetted. as reservoirs for arboviruses, and has experienced yellow Mosquito samples were placed immediately in labelled fever outbreaks [53]. Navrongo (urban site; 10°53′5″N, specimen bowls filled with water from the container 01°05′25″W) is a town close to the border between from which they had been collected, and transported to Ghana and Burkina Faso; an outbreak of dengue fever the insectary. Immature mosquitoes were reared in the was relatively recently reported in Burkina Faso, in the insectary in large white plastic trays at an average tem- period between 2016 and 2019 [54]. The last site was perature of 28.15 ± 1.8 °C (± SD) and relative humidity of Paga (suburban site; 10°59′32″N, 01°06′48″W), a small 80.9 ± 6.3%, and larvae were fed on TetraMin Baby fish town located on the border of Burkina Faso and 166 km food (Tetra Werke, Melle, Germany). south of Ouagadougou, where an outbreak of dengue Adult female Aedes mosquitoes that emerged from fever was recently reported [54] (Table 1). the collected larvae were used for the World Health In both the coastal savannah and forest area there is Organization (WHO) susceptibility bioassays [56] and generally a bimodal pattern of rainfall, with the long rainy later identified morphologically using standard taxo- season from April to June, and a short rainy season from nomic keys [57]. Coordinates of all collection points were October through November. Rainfall in the Sahel savan- recorded using a GPSMAP 60CSx Geographical Posi- nah is unimodal, with the rainy season between May and tioning System (GPS) instrument (Garmin International, November and the dry season from December to April. Olathe, KS). Sampling was done during the rainy season from April through June 2017 in the coastal savannah and forest Characterization of Aedes breeding habitats and relative zone, from May through June 2018 in the Sahel savan- abundance nah, during the dry season from January through March For each entomological survey, the habitat type, its 2018 in the coastal savannah and forested savannah, and household location (indoors or outdoors), and its physi- from December 2017 through January 2018 in the Sahel cal characteristics were recorded. Six container types savannah. were classified based on their use and material: car tyres, air conditioner saucers, discarded containers, drums, Distribution of immature Aedes mosquitoes tanks, and buckets. Air conditioner saucers are small Exhaustive entomological surveys were carried out at (1–2 L) plastic containers positioned below the outlet each of the study sites. Water-holding containers in of air conditioners to collect water. Discarded contain- and around human dwellings were inspected for imma- ers were defined as 50- to 100-L-capacity containers, ture Aedes in the dry and rainy seasons, and those posi- which included broken jars, bottles, small plastic food tive for Aedes immatures recorded. Larval habitats were containers, tins, plates, cans, cooking pots, and bro- sampled once per season. Every possible Aedes breeding ken pots made of plastic or metal. Drums were defined container was inspected for the presence of Aedes imma- as 100- to 500-L-capacity plastic water storage contain- tures at each site. Because it was difficult to sample most ers. Tanks were defined as 100- to 500-L-capacity water of the containers in which the Aedes bred by dipping, all storage containers made of metal or concrete. Buckets Aedes immatures encountered at each breeding habi- comprised 10- to 25-L water storage containers made of tat were collected to determine the density of vectors. metal or plastic. It is notable that pipeborne water was All pupae and larvae (first to fourth instars) from posi- absent in Larabanga and Paga, with the consequence tive containers (air conditioner saucers, car tyres, drums, that households tend to have long-term water storage in tanks, buckets, and discarded containers) were collected tanks, drums, buckets, and pots, especially during the dry Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 5 of 14 season, which may serve as potential Aedes larval breed- 3:00–7:00 p.m. The BG traps were baited with C O2 which ing habitats (Fig. 2). was produced by either BG-Lures and/or from a mixture of 17.5 g yeast [Angel Yeast (Egypt)] and 250 g sugar in Distribution of adult Aedes mosquitoes 1 L of water [59]. The mosquito collection net of the BG The spatial distribution of adult Aedes mosquitoes was trap was changed at 1-h intervals. Mosquitoes trapped determined by sampling inside households and outdoors. within the collection net were placed in a cooler box con- In the Sahel savannah zone, Aedes mosquitoes were sam- taining ice and then transported to the insectary. pled indoors and outdoors using three methods that The HLC method was also used to sample host-seeking employed one of the following: BG-Sentinel 2 traps (BG adult Aedes mosquitoes. On each day, two trained volun- traps; Biogents, Regensburg, Germany); human landing teers were positioned indoors and two were positioned catches (HLC); or Prokopack Aspirators (PPK) (Hock, outdoors to catch Aedes mosquitoes. The collected Aedes Gainesville, FL) [58]. The relative trapping efficiency of were placed in labelled paper cups, which were placed in the three sampling methods, i.e. using BG traps, HLC, or cool boxes with ice packs and transported to the insec- PPK, was compared for the Sahel savannah zone to deter- tary for identification and further processing. mine the most efficient vector sampling tool for future Prokopack aspiration was employed at the three sites in surveillance. Due to logistical challenges, in the coastal the Sahel savannah area: Larabanga, Navrongo, and Paga. and forest ecological zones, only two of the methods Sixteen houses were randomly selected for Aedes collec- were employed, the one which used BG traps and the one tion per site. Aedes mosquitoes were sampled indoors which used HLC. and outdoors. Aedes caught within the Prokopack plastic The GPS coordinates of all collection points were collection cups were labelled and placed in a cooler box recorded. Two cross-sectional surveys were undertaken, containing an ice pack and transported to the insectary one in the dry season (December 2017–March 2018) and for identification. The heights at which the mosquitoes one in the rainy season (April–June 2017 and May–June were caught by PPK while resting were recorded using a 2018). tape measure, to determine whether there was heteroge- neity in resting height among sites. Adult mosquito collection using BG traps, HLC and PPK Sixteen houses were randomly selected for each sam- BG traps were set both indoors [living room(s) and bed- pling method at each site. Sampling using each type of rooms] and outdoors (open but secure verandas, gra- sampling tool was done on 4 different days during each naries, or under a shed/tree where people sit to chat, season. On each of the sampling days, the houses used for about 5  m from the house) from 5:00 to 8:00 a.m. and sampling had not previously been used for this purpose. Fig. 2 Habitat types encountered during the larval survey and sampling: a air conditioner saucer, b car tyres, c buckets, d tank, e discarded container, and f drum Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 6 of 14 Mosquito sample collection using PPK and HLC was 24 h after the end of the bioassay, and ‘susceptible’ mos- done hourly from 5:00 to 8:00 a.m. and then from 3:00 to quitoes as those that were knocked down or died during 7:00 p.m. the 60-min exposure time, or that died within the 24-h Meetings were held at each study site with chiefs and recovery period. residents to introduce the research study to the public. All participants in this study were adults (> 18 years old). Data analysis Written and signed consent was obtained from all of the Descriptive analysis was performed to compare lar- adults who volunteered to participate in HLC before they val and adult abundance between different populations were trained and the mosquito sampling began. A copy (urban, suburban and rural), indoors and outdoors, and of the signed consent form was given to each of the HLC seasons. volunteers and another copy kept in a locked cabinet The abundances of Aedes larvae and adults were com- with restricted access in the offices of the Department pared among the seasons, indoor and outdoor study sites of Medical Microbiology, University of Ghana Medical (ecozones), and sampling methods (adults). For all sites, School. Verbal and written consent was obtained from a Kruskal–Wallis test was used to compare the abun- household heads to sample mosquitoes in their houses dance of adult mosquitoes for HLC and BG traps, and a and compounds. All volunteers were remunerated at the Wilcoxon rank-sum test was used to test for associations end of the study. between continuous and categorical variables. Nested generalized linear mixed models with sites nested within Insecticide susceptibility tests ecological zones were used to model the effect of ecoz- Aedes larvae were collected from natural breeding sites or one, season, population (urban, suburban and rural), from oviposition traps that were set in each site. Oviposi- and sampling methods on larval and adult abundance. A tion traps were made from used car tyres that had been regression analysis was done to test trap efficacy. Prob- cut into three parts which could hold about 3 L of water ability values less than 0.05 were interpreted as statisti- each. Oviposition traps were set for the collection of cally significant. Aedes immatures during time points when it was difficult Human blood index was calculated as the proportion to obtain sufficient numbers for the WHO susceptibility of positive human blood specimens per total number of bioassays. Collected larvae were brought to the insectary specimens tested. at the Department of Medical Microbiology, University Insecticide susceptibility was classified using the fol- of Ghana, and were raised to adults under standard con- lowing WHO criteria [56]: 98–100% mortality, the test ditions (25 ± 2 °C, 80% ± 4% relative humidity, 12-h:12-h population is considered susceptible; 90–97% mortality, light/dark cycle). Batches of 20–25 non-blood-fed 3- to possible resistance of the test population (which requires 5-day-old females were used for the susceptibility bioas- confirmation); below 90% mortality, the test population says. Four replicates and two controls were used for each is considered resistant. Knockdown and mortality rates insecticide tested using the standard WHO susceptibility were compared between sites using Chi-square. Statis- bioassay procedure [56]. tical analysis was performed using Stata 16 (StataCorp, The WHO test papers were impregnated with a pyre- College Station, TX). throid (0.05% deltamethrin or 0.75% permethrin), an organochloride [4% dichlorodiphenyltrichloroethane Results (DDT)], an organophosphate (5% malathion), or a carba- Larval breeding habitats and their productivity mate (0.1% bendiocarb) insecticide. These pre-impreg- A total of 81 positive breeding habitats were identified nated papers are supplied with diagnostic concentrations during the study period across the seven sites (only posi- based on those required for Anopheles. As the concentra- tive breeding habitats were recorded). Generalized linear tions of permethrin and malathion of the test papers are model analysis revealed a significant interaction effect three times and approximately six times, respectively, the between ecozone and population on abundance. Com- diagnostic concentrations required for Aedes mosquitoes, pared to the other sites, the chance of sampling Aedes this was a limitation of the study. However, these test larvae was higher in the forest zone [unadjusted (unadj.) papers are far more commonly used for the assessment B = − 204.12 (− 306.01 to − 102.24), P = 0.000]. The of the susceptibility of Aedes to these insecticides than abundance of Aedes larvae was higher in suburban areas those custom produced at the recommended concen- [unadj. B = − 138.01 (− 224.77 to − 51.26), P = 0.002] trations [60]. The knockdown time was reported every than in urban areas (Table 2). 10  min during the 60-min exposure period. Mortality There were significantly more positive habitats dur- was recorded after the 24-h recovery period. ‘Resistant’ ing the rainy season than during the dry season (n = 50 mosquitoes were defined as mosquitoes that survived for vs n = 31; df = 5, χ2 = 19.44, P = 0.001; Table  3). Within O wusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 7 of 14 Table 2 Factors associated with the productivity of larval habitats and larval abundance Characteristics Category Unadjusted B (CI) P-value Adjusted B (CI) P‑value Season Dry 1 1 Rainy 80.51 (− 2.26 to 163.27) 0.057 65.22 (− 12.02 to 142.46) 0.098 Ecozone Coastal savannah 1 1 Forest − 204.12 (− 306.01 to − 102.24) 0.000 − 184.81 (− 358.62 to − 10.99) 0.037 Sahel savannah − 72.9569 (− 157.57 to 11.65) 0.091 − 61.23 (− 158.68 to 36.21) 0.218 Indoors/outdoors Indoors 1 1 Outdoors 61.94 (− 155.38 to 279.25) 0.576 30.59 (− .194.75 to 255.92) 0.790 Population Urban 1 1 Suburban 8.62 (− 96.67 to 113.90) 0.873 13.89 (− 88.91 to 116.71) 0.791 Rural − 138.01 (− 224.77 to − 51.26) 0.002 − 9.43 (− 156.49 to 137.63) 0.900 CI Confidence interval Table 3 Seasonal distribution of positive breeding habitats by location and season Container type Season Location Total (%) Dry (%) Rainy (%) Indoors (%) Outdoors (%) Tyre 26 (44.07) 33 (55.93) 0 59 59 (100.00) Container 0 15 (100.00) 0 15 15 (100.00) Bucket 2 (100.00) 0 2 0 2 (100.00) Tank 0 1 (100.00) 0 1 1 (100.00) Drum 0 1(100.00) 1 0 1 (100.00) Air conditioner saucer 3 (100.00) 0 0 3 3 (100.00) Total 31 (38.27) 50 (61.73) 3 (3.7) 78 (96.3) 81 (100.00) the seven sites sampled, 78 (96.3%) of the larval breeding suburban areas, with a total of 3890 (23.3%) (Paga, 2079; habitats were located outdoors and three (3.7%) indoors Ada Foah, 1811), and then rural areas, with a total abun- (all in Larabanga) (Table  3), with larval abundances of dance of 1945 (11.6%) (Larabanga, 1945) (χ2 = 10.040, 16,426 (98.3%) and 285 (1.7%), respectively (n = 78 vs df = 2, P = 0.0066). We found more Aedes immatures n = 3; z = − 0.138, P = 0.8903). outdoors (16,426; 98.3%) than indoors (285; 1.7%) A total of 16,711 Aedes immatures were collected over (z = − 0.138, P = 0.8903). the entire sampling period, of which 12,348 (73.9%) were from car tyres, 3138 (18.8%) from discarded contain- Seasonal distribution of adult Aedes mosquitoes ers, 730 (4.4%) from air conditioner saucers, 230 (1.4%) A total of 1895 adult Aedes mosquitoes were collected from buckets, 210 (1.3%) from tanks, and 55 (0.3%) from the study sites. Generalized linear model analy- from drums (χ2 = 1.020, df = 5, P = 0.96; Table 4). For all sis revealed a significant interaction effect between the different sites, car tyres had the highest proportion, outdoor collection, ecozone and population (urban, 71.3% (8453), of immatures during the rainy season. The suburban, and rural) on abundance. The chance of same observation was made during the dry season, with sampling adult Aedes mosquitoes increased outdoors the highest abundance of Aedes immatures, 3895 (80.2%) [adj. B = 1.49 (1.0271–1.9602), P = 0.000]. There was (χ2 = 2.106, df = 2, P = 0.3490; Table 4), in car tyres. a significant difference between adult Aedes mosquito Regarding the different ecological zones, significantly abundance in suburban sites [adj. B = − 1.49 (− 2.0433 more Aedes immatures were collected from the coastal to − 0.9320), P = 0.000] and urban sites (Table 5). Adult savannah (9819; 58.8%), followed by the Sahel savan- Aedes were more abundant during the rainy season nah (5794; 34.7%), and then the forest zone (1098; 6.6%) (1257; 66.3%) compared to the dry season (638; 33.7%) (χ2 = 16.071, df = 2, P = 0.0003). A higher proportion of (z = − 1.433, P = 0.1519). Across the different ecological immature Aedes was collected in urban areas, with an zones, the abundance of Aedes was high in the coastal abundance of 10,876 (65.1%) (Tema, 4338; Accra, 3670; savannah (955; 50.4%) [Accra (urban), 718; Tema Navrongo, 1770; Konongo, 1098), followed by the (urban), 161; Ada Foah (suburban), 76], followed by the Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 8 of 14 Table 4 Productivity profile (number of Aedes immatures) of container type per site and season Container type Season Ada Foah Tema Accra Konongo Larabanga Navrongo Paga Car tyres Dry 695 2260 535 0 405 0 0 Rainy 1066 2078 487 558 505 1680 2079 Discarded containers Dry 0 0 0 0 0 0 0 Rainy 50 0 1918 540 540 90 0 Air conditioner saucer Dry 0 0 730 0 0 0 0 Rainy 0 0 0 0 0 0 0 Bucket Dry 0 0 0 0 230 0 0 Rainy 0 0 0 0 0 0 0 Tank Dry 0 0 0 0 0 0 0 Rainy 0 0 0 0 210 0 0 Drum Dry 0 0 0 0 0 0 0 Rainy 0 0 0 0 55 0 0 Seasonal totals Dry 695 2260 1265 0 635 0 0 Rainy 1116 2078 2405 1098 1310 1770 2079 Total 1811 4338 3670 1098 1945 1770 2079 Table 5 Factors associated with adult Aedes mosquito abundance Characteristics Category Unadjusted B (CI) P-value Adjusted B (CI) P‑value Season Dry 1 1 Rainy 0.34 (− 0.1487 to 0.8221) 0.174 0.49 (− 0.0109 to 0.9931) 0.055 Ecozone Coastal savannah 1 1 Forest − 0.44 (− 1.3873 to 0.5069) 0.362 − 1.16 (− 2.1213 to − 0.2186) 0.016 Sahel savannah − .16 (− 0.6561 to 0.3312) 0.519 0.19 (− 0.3609 to 0.746917) 0.495 Indoors/outdoors Indoors 1 1 Outdoors 1.45 (0.9840–1.9242) 0.000 1.49 (1.0271–1.9602) 0.000 Population Urban 1 1 Suburban − 1.25 (− 1.8001 to − 0.7042) 0.000 − 1.49 (− 2.0433 to − 0.9320) 0.000 Rural − 1.49 (− 2.1720 to − 0.8260) 0.000 − 1.844 (− 2.5952 to − 1.0935) 0.000 Sahel savannah 837 (44.2%) [Navrongo (urban), 577; During the rainy season, the highest abundance of Paga (suburban), 173; Larabanga (rural), 87], and the Aedes mosquitoes was found in Accra (540; 43.0%) forest zone (103; 5.4%) [Konongo (urban), 103] ( χ (HLC, 499; BG trap, 41), followed by Navrongo (404; 2 = 0.359, df = 2, P = 0.835). The urban sites had the 32.1%) (HLC, 354; BG trap, 50), Paga (172; 13.7%) highest abundances of Aedes mosquitoes (1559, 82.3%) (HLC, 168; BG trap, 4), Larabanga (72; 5.7%) (HLC, 54; (Accra, 718; Tema, 161; Konongo, 103; Navrongo, 577) BG trap, 18), Tema (53; 4.2%) (HLC, 31; BG trap, 22), followed by the suburban sites (249; 13.1%) (Ada Ada Foah (16; 1.3%) (HLC, 0; BG trap, 16), and then Kon- Foah, 76; Paga, 173), and then the rural site (87; 4.6%) ongo (0, 0%) (HLC, 0; BG trap, 0), ( 2χ = 132.896, df = 6, (Larabanga, 87) ( 2χ = 20.147, df = 2, P = 0.0001). P = 0.0001). At the different sites during the dry season, the highest abundance of Aedes mosquitoes was found in Accra (178; Indoor and outdoor abundance of adult Aedes populations 27.9%) (HLC, 163; BG trap, 15), followed by Navrongo Overall mosquito abundance was highest outdoors as (173; (27.1%) (HLC, 157; BG trap, 16), Tema (108; 16.9%) compared to indoors over the entire sampling period. (HLC, 102; BG trap, 6), Konongo (103; 16.1%) (HLC, 88; Indoor sampling yielded a total of 381 (20.1%) and out- BG trap, 15), Ada (60; 9.4%) (HLC, 50; BG trap, 10), door sampling a total of 1514 (79.9%) adult Aedes over Larabanga (15; 2.4%) (HLC, 0; BG trap, 15), and then the entire sampling period (z = − 5.427, P = 0.0000). Dur- Paga (1; 0.2%) (HLC, 1; BG trap, 0) ( 2χ = 20.500, df = 6, ing the rainy season, a higher proportion of Aedes mos- P = 0.0023). quitoes was captured outdoors (77.8%; 978) than indoors O wusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 9 of 14 (22.2%; 279) (z = − 2.989, P = 0.0028). Similarly, a greater site and sampling method on abundance. More adult number of Aedes mosquitoes were captured outdoors Aedes mosquitoes were collected outdoors [adj. B = 0.87 (536; 84%) than indoors (102; 16%) during the dry season (0.22, 1.52), P = 0.009]. Adult Aedes mosquitoes were (z = − 5.021, P = 0.0000; Fig. 3). more abundant in Navrongo [adj. B = 0.83 (0.07, 1.58), P = 0.032], and BG traps were the least efficient means Comparison of trap efficiency for Aedes mosquito sampling of collecting Aedes mosquitoes [adj. B = − 1.39 (− 2.14, A total of 1140 Aedes mosquitoes were collected by HLC, − 0.64), P < 0.001; Table 7]. BG traps, and PPK in Larabanga, Navrongo, and Paga during the experiment. Overall, the abundance of adult Aedes mosquitoes was 2.4 times higher for HLC (734) Resting height of Aedes mosquitoes compared to PPK (303), and 7.1 times higher for HLC The maximum height at which Aedes mosquitoes were compared to BG traps (103). There was a significant dif- caught resting was 5  m and the lowest 1  m. The mean ference between the abundance of Aedes mosquitoes preferred resting height of the caught Aedes mosquitoes for HLC and BG traps [P = 0.000, 95% confidence inter- ranged from 1.8 to 2.0 m indoors and 1.3–2.8 m outdoors val (CI) = − 2.180248 to − 0.7245137], but no signifi- ( 2χ = 1.408, df = 2, P = 0.4945). No mosquito was caught cant difference between HLC and PPK (P = 0.350, 95% resting indoors in Navrongo (Table 8). CI = − 0.4820909 to 1.359284; Table 6). Generalized linear model analysis revealed a signifi- cant interaction effect between outdoor collection, study Fig. 3 Seasonal distribution of adult Aedes mosquitoes captured indoors (IN) and outdoors (OUT). BG BG‑Sentinel 2 trap, HLC human landing catches Table 6 Comparison of sampling methods for the collection of mosquitoes in the Sahel ecological zone Study sites Dry season Rainy season BG trap (%) HLC (%) PPK (%) BG trap (%) HLC (%) PPK (%) In. Out. In. Out. In. Out. In. Out. In. Out. In. Out. Larabanga 2 (13.3) 13 (86.7) 0 0 1 (4.4) 22 (95.6) 4 (22.2) 14 (77.8) 34 (63) 20 (37) 40 (32) 86 (68) Navrongo 10 (62.5) 6 (37.5) 36 (22.9) 121 (77.1) 0 22 (100) 18 (36) 32 (64) 92 (26) 262 (74) 0 8 (100) Paga 0 0 0 1 (100) 0 0 4 (100) 0 37 (22) 131 (78) 87 (70) 37 (30) Total 12 (5.1) 19 (8.1) 36 (15.4) 122 (52.1) 1 (0.4) 44 (18.8) 26 (2.8) 46 (5.1) 163 (18) 413 (45.6) 127 (14) 131 (14.5) Total per trap 31 (2.7) 158 (13.9) 45 (3.9) 72 (6.3) 576 (50.5) 258 (22.6) BG trap BG‑Sentinel 2 trap, HLC human landing catch, PPK Prokopack Aspirator, In. indoors, Out. outdoors Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 10 of 14 Aedes species composition at the study sites Blood meal analysis Morphological identification of all collected adult Blood meal analysis was carried out on blood-fed mos- Aedes showed that Aedes aegypti (1854; 97.8%) was quitoes that were sampled using BG traps and PPK in the most abundant species present at all sites followed Larabanga, Navrongo, and Paga. PCR amplification of by Aedes africanus (40; 2.1%) and Aedes luteocephalus DNA segments of 20 of 44 blood-fed mosquitoes showed (1; 0.01%) (Table 9). All 11,506 Aedes mosquitoes that that 18 (90%) had taken a human blood meal, one (5%) emerged from the larvae collected from the sites and had fed on a human and a cow, and one (5%) had taken reared in the insectary were identified morphologi- blood meals from a dog and a goat. cally as Aedes aegypti (Table 9). Phenotypic resistance of Aedes to insecticides Phenotypic test results showed that Aedes mosquito pop- ulations from all study sites were resistant to DDT (range Table 7 Factors associated with the capture efficiency of HLC, BG traps, and PPK Characteristics Category Unadjusted B (CI) P-value Adjusted B (CI) P‑value Season Dry 1 1 Rainy 0.31 (− 0.45, 1.08) 0.425 0.09 (− 0.71, 0.89) 0.821 Indoors/outdoors Indoors 1 1 Outdoors 0.90 (0.24, 1.56) 0.007 0. 87 (0.22, 1.52) 0.009 Site Larabanga 1 1 Navrongo 0.98 (0.22, 1.74) 0.011 0.83 (0.07, 1.58) 0.032 Paga 0.65 (− 0.22, 1.52) 0.142 0.34 (− 0.54, 1.23) 0.446 Trap HLC 1 1 BG trap − 1.45 (− 2.18, − 0.72) 0.0001 − 1.39 (− 2.14, − 0.64) 0.000 PPK 0.44 (− 0.48, 1.36) 0.350 0.42 (− 0.50, 1.34) 0.373 For abbreviations, see Tables 2 and 6 Table 8 Resting heights of Aedes per study site Study site Total number of Total number of Total number Highest height Average mosquito Average mosquito mosquitoes (%) mosquitoes indoors of mosquitoes of houses (m) resting height (indoors) resting height outdoors (m) (outdoors) (m) Paga 124 (48.1) 87 37 4 1.8 1.3 Navrongo 8 (3.1) 0 8 5 – 2.8 Larabanga 126 (48.8) 40 86 5 2.0 2.4 Table 9 Number of Aedes mosquitoes per study site identified morphologically to species level Study site Adults Larvaea Total per site (%) Aedes aegypti (%) Aedes africanus (%) Aedes luteocephalus (%) Aedes aegypti (%) Ada Foah 76 (100.0) 64 (84.2) 12 (15.8) 0 (0.0) 981 (100.0) Tema 161 (100.0) 161 (100.0) 0 (0.0) 0 (0.0) 3021 (100.0) Accra 718 (100.0) 718 (100.0) 0 (0.0) 0 (0.0) 2650 (100.0) Konongo 103 (100.0) 80 (77.7) 23 (22.3) 0 (0.0) 1098 (100.0) Larabanga 87 (100.0) 83 (95.4) 3 (3.4) 1 (1.1) 1196 (100.0) Navrongo 577 (100.0) 575 (99.7) 2 (0.3) 0 (0.0) 795 (100.0) Paga 173 (100.0) 173 (100.0) 0 (0.0) 0 (0.0) 1765 (100.0) Total 1895 (100) 1854 (97.8) 40 (2.1) 1 (0.1) 11,506 (100.0) a Raised to adult stage in the insectary O wusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 11 of 14 0–88%). The highest level of DDT resistance was seen in Appawu et al. [53] showed an increase in the abundance Tema, where none of the mosquitoes died on exposure to of Aedes immatures during the dry season in Ghana. this insecticide. The vectors showed resistance to perme- Car tyres, buckets, tanks, drums, discarded containers, thrin in Tema (21%), Accra (40.0%) and Larabanga (89%), and air conditioner saucers that had collected water were and suspected resistance in Navrongo (90%), Paga (96%) the main breeding sites and supported the development and Konongo (90%) (χ 2 = 1.331, df = 12, P = 0.0001). of Aedes immatures in all or some of the study sites. The Aedes mosquitoes showed resistance to deltamethrin in distribution of Aedes immatures between container types Tema (68%) and suspected resistance in Accra (91.3%), varied between the dry and rainy seasons. In all, only car Ada Foah (94%), Konongo (94%), Larabanga (93%), tyres could be considered key breeding habitats in both Navrongo (96%) and Paga (93%) ( 2χ = 560.000, df = 6, seasons at all sites, and over 70% of the Aedes immatures P = 0.0001). Aedes mosquitoes were resistant to bendio- were collected from these during the study period. The carb in Larabanga (81%), showed suspected resistance in abundance of Aedes immatures in car tyres found here is Tema (95.0%), Konongo (96%), Navrongo (96%) and Paga consistent with the findings of a study conducted in the (97%), and were susceptible to bendiocarb in Accra and Central African Republic [63], where used car tyres were Ada Foah ( 2χ = 1.331, df = 12, P = 0.0001). Aedes mos- the most heavily colonized and productive larval habitats quitoes were susceptible to the organophosphate (mala- for Aedes in both early and late wet seasons. Car tyres thion) at all sites (Fig. 4). should therefore be targeted for vector control to elimi- nate most Aedes immatures. Habitats that were non- productive were not included in this study. Larval indices Discussion (container index, house index, and Breteau index) were Seasonal variation in population density is common for not calculated because we did not record habitats that Aedes mosquitoes due to their sensitivity to changes in did not have larvae in them, which was a major limitation temperature and moisture [53, 61]. This study found a of this study. significantly higher abundance of Aedes immatures dur- The WHO susceptibility bioassays showed that Aedes ing the rainy season. The rains may have resulted in an mosquito populations from all of the study sites were increase in aquatic habitats for Aedes spp. that breed in resistant to DDT. This finding is similar to that of a previ- car tyres and the other types of suitable containers that ous study done in Accra, Ghana, which showed that Ae. were encountered in this study [62], and thus an increase aegypti were resistant to DDT [64]. Deltamethrin, per- in the abundance of Aedes immatures due to an increase methrin, and bendiocarb resistance were also recorded in in the rate of oviposition. This finding was similar to that the present study. As these are some of the most widely of Ngugi et  al. [39], who found a higher abundance of used insecticides for the control of Aedes spp. [65, 66], immatures during the rainy season in Kenya. However, their use in Ghana could negatively affect the efficacy of Fig. 4 Phenotypic resistance status of Aedes mosquitoes to different insecticides. DDT Dichlorodiphenyltrichloroethane Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 12 of 14 vector control efforts there. Deltamethrin and perme- implications for the efficacy of indoor residual spraying thrin resistance could result from the widespread use due to the exophilic behaviours of some Aedes mosqui- of pyrethroids for the impregnation of bed nets and for toes. Insecticide pressure indoors through indoor resid- indoor residual spraying against malaria vectors. Pyre- ual spraying may also trigger exophagy and thus outdoor throid resistance has been recently reported in an Aedes transmission of arboviruses. population in Ghana [64]. Cross-resistance between pyrethroids and DDT is also known to occur [29]. A previous study in Ghana [64] found Aedes to be suscep- Conclusions tible to permethrin. Other studies have also reported The results of this study indicate that breeding habitats pyrethroid resistance in Aedes spp. in Africa and Asia of Ae. aegypti in Ghana are abundant outdoors and are [67–69]. diverse across the country. Car tyres were the most pro- In this study, Ae. aegypti was the predominant spe- ductive containers for Aedes, as > 70% of the Aedes larvae cies in all of the study areas for both adult and larval were collected from these. Thus, targeting tyres in source sampling. The high number of Ae. aegypti caught from reduction efforts may be a cost-effective means of reduc- a geographically wide range of sites in different ecologi- ing the risk of arboviral disease transmission in Ghana. cal zones may be explained by the behaviour of this spe- Resistance of Ae. aegypti to pyrethroids and carbamates cies, which is highly anthropophilic and associated with requires careful monitoring as it could limit the efficacy human habitations, as reported by many studies under- of vector control programmes. Management strate- taken in Central Africa and West Africa [64, 68, 70]. The gies for vector control that take into account insecticide high abundance of Ae. aegypti observed in the present resistance are thus urgently needed for Ghana. study implies that this vector of yellow fever and dengue is well established in Ghana, which could increase the Abbreviations potential for the transmission of arboviral diseases across BG: BG‑Sentinel 2; DDT: Dichlorodiphenyltrichloroethane; GPS: Geographical the country because outbreaks of these are more severe Positioning System; HLC: Human landing catch; PPK: Prokopack Aspirator; WHO: World Health Organization. in the absence of effective vector control. This calls for constant vector monitoring in Ghana to Acknowledgements prevent outbreaks of arboviral diseases. The zoonotic We thank the residents of the study sites for their support during our study. Our sincere gratitude goes to Dr Victor Asoala, Stephen Kantum, and Bernice Aedes species Ae. africanus and Ae. luteocephalus, which Ama Baako; all of the staff of the Entomology Department of the Navrongo are involved in sylvatic cycles between non-human pri- Health Research Centre, Ghana; Mr Sylvester Coleman of the President Malaria mates, were also found in this study, which suggests that Initiative, Tamale; and Mr Isaac K. Sraku and Prince Ashong‑Pappoe of the Medical Microbiology Department, University of Ghana for field and labora‑ they may act as bridge vectors and carry disease between tory assistance. sylvan and domestic environments, as both are vectors of yellow fever in Ghana [64]. In addition, Hanley et  al. Authors’ contributions CMO‑A, JAAM, DW, and YAA were responsible for the study design, supervised [71] reported that Ae. africanus is the primary vector the data collection, and contributed to the writing of the manuscript. CMO‑A of sylvatic yellow fever virus in the rainforests of Cen- performed the data collection and analysis, laboratory work, and drafted the tral Africa, extending outward along the riverine forests manuscript. All the authors read and approved the final manuscript. there, and Diallo et  al. [72] detected yellow fever in the Funding zoonotic species Ae. luteocephalus in Senegal. Suzuki This study was supported by grants from the National Institute of Health (D43 et al. [64] found only one Ae. albopictus in Accra, Ghana, TW 011513). and in our current study we did not find any individuals Availability of data and materials of this species in any of the study sites. The absence of All datasets generated and/or analysed during this study are available on this species from our samples suggests that environmen- request. tal factors in Ghana may not be favourable for its estab- lishment and proliferation. The dominance of its sister Declarations species, Ae. aegypti, may result from favourable environ- Ethics approval and consent to participate mental conditions for its proliferation. This study was approved by the Ethics and Protocol Review Committee of the The present study showed that Ae. aegypti rests at an College of Health Sciences of the University of Ghana (protocol identification number CHS‑Et/M.9‑P1.5/2017–2018). Meetings were held at each study site average height of 1.8–2.0 m indoors and 1.3–2.8 m out- with the chiefs and the residents to introduce the research study to the public. doors. These observations are quite different from those All study participants were adults (at least 18 years old). Written and signed of studies undertaken in Iquitos, Peru [58] and Aca- consent was obtained from all the adults who volunteered to participate in HLC sampling before they were trained and the sampling of mosquitoes pulco, Mexico [73], which showed that of 56 and 626 Ae. commenced. A copy of their signed consent form was given to each of the aegypti collected indoors, respectively, 82% rested at a HLC volunteers and another copy kept in a locked cabinet with restricted height of less than 1.5 m. Resting height may have major access in the offices of the Department of Medical Microbiology, University of Ghana Medical School. Verbal consent was obtained from household heads Owusu‑Asenso et al. Parasites & Vectors (2022) 15:61 Page 13 of 14 to sample mosquitoes in their houses and compounds. Ethical approval for 15. World Health Organisation b. Yellow fever—Senegal. WHO. 2021. https:// the use of volunteers for mosquito sampling and the protocols involved was www.w ho.i nt/c sr/ don/ 29‑ decem ber‑2 020‑ yellow‑ fever‑ seneg al/ en/. sought from the Ethics and Protocol Review Committee of the College of Assessed 29 Dec 2020. Health Sciences of the University of Ghana (protocol identification number 16. World Health Organisation c. Yellow fever—Guinea. WHO. 2021. https:// CHS‑Et/M.9‑P1.5/2017–2018). Permission to carry out the study at the various www. who. int/ csr/d on/ 23‑ decem ber‑2 020‑ yellow‑ fever‑g uinea/e n/. study sites was sought from community leaders, and verbal consent was Assessed 23 Dec 2020. sought from the heads of households before houses were entered for inspec‑ 17. Stoler J, Delimini RK, Bonney JH, Oduro AR, Owusu‑Agyei S, Fobil JN, tion and sampling. et al. Evidence of recent dengue exposure among malaria parasite‑ positive children in three urban centers in Ghana. Am J Trop Med Hyg. Consent for publication 2015;92:497–500. Not applicable. 18. Amoako N, Duodu S, Dennis FE, Bonney JHK, Asante KP, Ameh J, et al. Detection of dengue virus among children with suspected malaria, Accra. Competing interests Ghana Emerg Infect Dis. 2018;24:1544–7. The authors declare that they have no competing interests. 19. Bonney JHK, Hayashi T, Dadzie S, Agbosu E, Pratt D, Nyarko S, et al. Molecular detection of dengue virus in patients suspected of Ebola virus Author details disease in Ghana. PLoS ONE. 2018;13:e0208907. 1 Department of Medical Microbiology, University of Ghana Medical School, 20. Manu SK, Bonney JHK, Pratt D, Abdulai FN, Agbosu EE, Frimpong PO, et al. University of Ghana, Korle‑Bu, Accra, Ghana. 2 Department of Vector Biology, Arbovirus circulation among febrile patients at the greater Accra Regional Liverpool School of Tropical Medicine, Liverpool, UK. Hospital, Ghana. BMC Res Notes. 2019;12:332. 21. Scott TW, Takken W. Feeding strategies of anthropophilic mosquitoes Received: 13 October 2021 Accepted: 25 January 2022 result in increased risk of pathogen transmission. Trends Parasitol. 2012;28:114–21. 22. Lounibos LP. Invasions by insect vectors of human disease. Annu Rev Entomol. 2002;47:233–66. 23. Brown JE, McBride CS, Johnson P, Ritchie S, Paupy C, Bossin H, et al. 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Choose BMC and benefit from: int/ iris/ bitst ream/ handle/1 0665/ 250677/ 97892 41511 575‑e ng. pdf? seque nce= • fast, convenient online submission1. Assessed 15 Jan 2017. 57. Huang Y‑M. The subgenus Stegomyia of Aedes in the Afrotropical region • thorough peer review by experienced rese archers in your field with keys to the species (Diptera: Culicidae). Zootaxa. 2004;700:1–120. • rapid publication on acceptance 58. Vazquez‑Prokopec GM, Galvin WA, Kelly R, Kitron U. A new, cost‑effective, • support for research data, including large and complex data types battery‑powered aspirator for adult mosquito collections. J Med Entomol. 2009;46:1256–9. • gold Open Access which fosters wider collaboration and increased citations 59. Ndenga BA, Mutuku FM, Ngugi HN, Mbakaya JO, Aswani P, Musunzaji PS, • maximum visibility for your research: over 100M website views per year et al. Characteristics of Aedes aegypti adult mosquitoes in rural and urban areas of western and coastal Kenya. PLoS ONE. 2017;12:e0189971. At BMC, research is always in progress. 60. Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, et al. Con‑ temporary status of insecticide resistance in the major Aedes vectors of Learn more biomedcentral.com/submissions arboviruses infecting humans. PLOS Negl Trop Dis. 2017;11:e0005625.