Dataset Information

Linking human behaviours and malaria vector biting risk in south-eastern Tanzania.

ABSTRACT: To accelerate malaria elimination in areas where core interventions such as insecticide-treated nets (ITNs) are already widely used, it is crucial to consider additional factors associated with persistent transmission. Qualitative data on human behaviours and perceptions regarding malaria risk was triangulated with quantitative data on Anopheles mosquito bites occurring indoors and outdoors in south-eastern Tanzania communities where ITNS are already used but lower level malaria transmission persists. Each night (18:00h-07:00h), trained residents recorded human activities indoors, in peri-domestic outdoor areas, and in communal gatherings. Host-seeking mosquitoes were repeatedly collected indoors and outdoors hourly, using miniaturized exposure-free double net traps (DN-Mini) occupied by volunteers. In-depth interviews were conducted with household representatives to explore perceptions on persistent malaria and its control. Higher proportions of people stayed outdoors than indoors in early-evening and early-morning hours, resulting in higher exposures outdoors than indoors during these times. However, exposure during late-night hours (22:00h-05:00h) occurred mostly indoors. Some of the popular activities that kept people outdoors included cooking, eating, relaxing and playing. All households had at least one bed net, and 83.9% of people had access to ITNs. Average ITN use was 96.3%, preventing most indoor exposure. Participants recorgnized the importance of ITNs but also noted that the nets were not perfect. No complementary interventions were reported being used widely. Most people believed transmission happens after midnight. We conclude that insecticide-treated nets, where properly used, can still prevent most indoor exposures, but significant risk continues unabated before bedtime, outdoors and at communal gatherings. Such exposure is greatest for rural and low-income households. There is therefore an urgent need for complementary interventions, particularly those targeting outdoor-biting and are applicable for all people including the marginalised populations such as migratory farmers and fishermen. Besides, the differences in community understanding of ongoing transmission, and feedback on imperfections of ITNs should be considered when updating malaria-related communication and interventions.

SUBMITTER: Finda MF

PROVIDER: S-EPMC6546273 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Linking human behaviours and malaria vector biting risk in south-eastern Tanzania.

Finda Marceline F MF Moshi Irene R IR Monroe April A Limwagu Alex J AJ Nyoni Anna P AP Swai Johnson K JK Ngowo Halfan S HS Minja Elihaika G EG Toe Lea P LP Kaindoa Emmanuel W EW Coetzee Maureen M Manderson Lenore L Okumu Fredros O FO

PloS one 20190603 6

To accelerate malaria elimination in areas where core interventions such as insecticide-treated nets (ITNs) are already widely used, it is crucial to consider additional factors associated with persistent transmission. Qualitative data on human behaviours and perceptions regarding malaria risk was triangulated with quantitative data on Anopheles mosquito bites occurring indoors and outdoors in south-eastern Tanzania communities where ITNS are already used but lower level malaria transmission per ...[more]

PMID: 31158255

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Project description:BackgroundThe use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucidation of the mechanisms behind these shifts is crucial for anticipating impacts on vector control.MethodsA novel portable semi-field system (PSFS) was used to experimentally measure heritability of biting time in the malaria vector Anopheles arabiensis in Tanzania. Wild An. arabiensis from hourly collections using the human landing catch (HLC) method were grouped into one of 3 categories based on their time of capture: early (18:00-21:00), mid (22:00-04:00), and late (05:00-07:00) biting, and placed in separate holding cages. Mosquitoes were then provided with a blood meal for egg production and formation of first filial generation (F1). The F1 generation of each biting time phenotype category was reared separately, and blood fed at the same time as their mothers were captured host-seeking. The resultant eggs were used to generate the F2 generation for use in heritability assays. Heritability was assessed by releasing F2 An. arabiensis into the PSFS, recording their biting time during a human landing catch and comparing it to that of their F0 grandmothers.ResultsIn PSFS assays, the biting time of F2 offspring (early: 18:00-21:00, mid: 22:00-04:00 or late: 05:00-07:00) was significantly positively associated with that of their wild-caught F0 grandmothers, corresponding to an estimated heritability of 0.110 (95% CI 0.003, 0.208). F2 from early-biting F0 were more likely to bite early than F2 from mid or late-biting F0. Similarly, the probability of biting late was higher in F2 derived from mid and late-biting F0 than from early-biting F0.ConclusionsDespite modest heritability, our results suggest that some of the variation in biting time is attributable to additive genetic variation. Selection can, therefore, act efficiently on mosquito biting times, highlighting the need for control methods that target early and outdoor biting mosquitoes.

Project description:Subsistence rice farmers in south-eastern Tanzania are often migratory, spending weeks or months tending to crops in distant fields along the river valleys and living in improvised structures known as Shamba huts, not fully protected from mosquitoes. These farmers also experience poor access to organized preventive and curative services due to long distances. Mosquito biting exposure in these rice fields, relative to main village residences was assessed, then a portable mosquito-proof hut was developed and tested for protecting these migratory farmers.Pair-wise mosquito surveys were conducted in four villages in Ulanga district, south-eastern Tanzania in 20 randomly-selected Shamba huts located in the distant rice fields and in 20 matched houses within the main villages, to assess biting densities and Plasmodium infection rates. A portable mosquito-proof hut was designed and tested in semi-field and field settings against Shamba hut replicas, and actual Shamba huts. Also, semi-structured interviews were conducted, timed-participant observations, and focus-group discussions to assess experiences and behaviours of the farmers regarding mosquito-bites and the mosquito-proof huts.There were equal numbers of mosquitoes in Shamba huts and main houses [RR (95% CI) 27 (25.1-31.2), and RR (95% CI) 30 (27.5-33.4)], respectively (P > 0.05). Huts having >1 occupant had more mosquitoes than those with just one occupant, regardless of site [RR (95% CI) 1.57 (1.30-1.9), P < 0.05]. Open eaves [RR (95% CI) 1.15 (1.08-1.23), P < 0.05] and absence of window shutters [RR (95% CI) 2.10 (1.91-2.31), P < 0.05] increased catches of malaria vectors. All Anopheles mosquitoes caught were negative for Plasmodium. Common night-time outdoor activities in the fields included cooking, eating, fetching water or firewood, washing dishes, bathing, and storytelling, mostly between 6 and 11 p.m., when mosquitoes were also biting most. The prototype hut provided 100% protection in semi-field and field settings, while blood-fed mosquitoes were recaptured in Shamba huts, even when occupants used permethrin-impregnated bed nets.Though equal numbers of mosquitoes were caught between main houses and normal Shamba huts, the higher proportions of blood-fed mosquitoes, reduced access to organized healthcare and reduced effectiveness of LLINs, may increase vulnerability of the itinerant farmers. The portable mosquito-proof hut offered sufficient protection against disease-transmitting mosquitoes. Such huts could be improved to expand protection for migratory farmers and possibly other disenfranchised communities.

Project description:Background: Programmatic monitoring of insecticide resistance in disease vectors is mostly done on a large scale, often focusing on differences between districts, regions or countries. However, local heterogeneities in residual malaria transmission imply the need for finer-scale data. This study reports small-scale variations of insecticide susceptibility in Anopheles arabiensis between three neighbouring villages across two seasons in Tanzania, where insecticidal bed nets are extensively used, but malaria transmission persists. Methods: WHO insecticide susceptibility assays were conducted on female and male An. arabiensis from three proximal villages, Minepa, Lupiro, and Mavimba, during dry (June-December 2015) and wet (January-May 2016) seasons. Adults emerging from wild-collected larvae were exposed to 0.05% lambda-cyhalothrin, 0.05% deltamethrin, 0.75% permethrin, 4% DDT, 4% dieldrin, 0.1% bendiocarb, 0.1% propoxur, 0.25% pirimiphos-methyl and 5% malathion. A hydrolysis probe assay was used to screen for L1014F ( kdr-w) and L1014S ( kdr-e) mutations in specimens resistant to DDT or pyrethroids. Synergist assays using piperonly butoxide (PBO) and triphenol phosphate (TPP) were done to assess pyrethroid and bendiocarb resistance phenotypes. Results: There were clear seasonal and spatial fluctuations in phenotypic resistance status in An. arabiensis to pyrethroids, DDT and bendiocarb. Pre-exposure to PBO and TPP, resulted in lower knockdown rates and higher mortalities against pyrethroids and bendiocarb, compared to tests without the synergists. Neither L1014F nor L1014S mutations were detected. Conclusions: This study confirmed the presence of pyrethroid resistance in An. arabiensis and showed small-scale differences in resistance levels between the villages, and between seasons. Substantial, though incomplete, reversal of pyrethroid and bendiocarb resistance following pre-exposure to PBO and TPP, and absence of kdr alleles suggest involvement of P450 monooxygenases and esterases in the resistant phenotypes. We recommend, for effective resistance management, further bioassays to quantify the strength of resistance, and both biochemical and molecular analysis to elucidate specific enzymes responsible in resistance.

Project description:BACKGROUND:Malaria control in Africa relies extensively on indoor residual spraying (IRS) and insecticide-treated nets (ITNs). IRS typically targets mosquitoes resting on walls, and in few cases, roofs and ceilings, using contact insecticides. Unfortunately, little attention is paid to where malaria vectors actually rest indoors, and how such knowledge could be used to improve IRS. This study investigated preferred resting surfaces of two major malaria vectors, Anopheles funestus and Anopheles arabiensis, inside four common house types in rural south-eastern Tanzania. METHODS:The assessment was done inside 80 houses including: 20 with thatched roofs and mud walls, 20 with thatched roofs and un-plastered brick walls, 20 with metal roofs and un-plastered brick walls, and 20 with metal roofs and plastered brick walls, across four villages. In each house, resting mosquitoes were sampled in mornings (6 a.m.-8 a.m.), evenings (6 p.m.-8 p.m.) and at night (11 p.m.-12.00 a.m.) using Prokopack aspirators from multiple surfaces (walls, undersides of roofs, floors, furniture, utensils, clothing, curtains and bed nets). RESULTS:Overall, only 26% of An. funestus and 18% of An. arabiensis were found on walls. In grass-thatched houses, 33-55% of An. funestus and 43-50% of An. arabiensis rested under roofs, while in metal-roofed houses, only 16-20% of An. funestus and 8-30% of An. arabiensis rested under roofs. Considering all data together, approximately 40% of mosquitoes rested on surfaces not typically targeted by IRS, i.e. floors, furniture, utensils, clothing and bed nets. These proportions were particularly high in metal-roofed houses (47-53% of An. funestus; 60-66% of An. arabiensis). CONCLUSION:While IRS typically uses contact insecticides to target adult mosquitoes on walls, and occasionally roofs and ceilings, significant proportions of vectors rest on surfaces not usually sprayed. This gap exceeds one-third of malaria mosquitoes in grass-thatched houses, and can reach two-thirds in metal-roofed houses. Where field operations exclude roofs during IRS, the gaps can be much greater. In conclusion, there is need for locally-obtained data on mosquito resting behaviours and how these influence the overall impact and costs of IRS. This study also emphasizes the need for alternative approaches, e.g. house screening, which broadly tackle mosquitoes beyond areas reachable by IRS and ITNs.

Project description:The biting cycle of anopheline mosquitoes is an important component in the transmission of malaria. Inter- and intraspecific biting patterns of anophelines have been investigated using the number of mosquitoes caught over time to compare general tendencies in host-seeking activity and cumulative catch. In this study, all-night biting catch data from 32 consecutive months of collections in three riverine villages were used to compare biting cycles of the five most abundant vector species using common statistics to quantify variability and deviations of nightly catches from a normal distribution.Three communities were selected for study. All-night human landing catches of mosquitoes were made each month in the peridomestic environment of four houses (sites) for nine consecutive days from April 2003 to November 2005. Host-seeking activities of the five most abundant species that were previously captured infected with Plasmodium falciparum, Plasmodium malariae or Plasmodium vivax, were analysed and compared by measuring the amount of variation in numbers biting per unit time (co-efficient of variation, V), the degree to which the numbers of individuals per unit time were asymmetrical (skewness = g1) and the relative peakedness or flatness of the distribution (kurtosis = g2). To analyse variation in V, g1, and g2 within species and villages, we used mixed model nested ANOVAs (PROC GLM in SAS) with independent variables (sources of variation): year, month (year), night (year X month) and collection site (year X month).The biting cycles of the most abundant species, Anopheles darlingi, had the least pronounced biting peaks, the lowest mean V values, and typically non-significant departures from normality in g1 and g2. By contrast, the species with the most sharply defined crepuscular biting peaks, Anopheles marajoara, Anopheles nuneztovari and Anopheles triannulatus, showed high to moderate mean V values and, most commonly, significantly positive skewness (g1) and kurtosis (g2) moments. Anopheles intermedius was usually, but not always, crepuscular in host seeking, and showed moderate mean V values and typically positive skewness and kurtosis. Among sites within villages, significant differences in frequencies of departures from normality (g1 and g2) were detected for An. marajoara and An. darlingi, suggesting that local environments, such as host availability, may affect the shape of biting pattern curves of these two species.Analyses of co-efficients of variation, skewness and kurtosis facilitated quantitative comparisons of host-seeking activity patterns that differ among species, sites, villages, and dates. The variable and heterogeneous nightly host-seeking behaviours of the five exophilic vector species contribute to the maintenance of stable malaria transmission in these Amazonian villages. The abundances of An. darlingi and An. marajoara, their propensities to seek hosts throughout the night, and their ability to adapt host-seeking behaviour to local environments, contribute to their impact as the most important of these vector species.

Project description:BackgroundAnopheles calderoni was first recognized in Colombia in 2010 as this species had been misidentified as Anopheles punctimacula due to morphological similarities. An. calderoni is considered a malaria vector in Peru and has been found naturally infected with Plasmodium falciparum in Colombia. However, its biting behaviour, population dynamics and epidemiological importance have not been well described for Colombia.MethodsTo assess the contribution of An. calderoni to malaria transmission and its human biting behaviour and spatial/temporal distribution in the southwest of Colombia, human landing catches (HLC) and larval collections were carried out in a cross-sectional, entomological study in 22 localities between 2011 and 2012, and a longitudinal study was performed in the Boca de Prieta locality in Olaya Herrera municipality between July 2012 and June 2013. All mosquitoes determined as An. calderoni were tested by ELISA to establish infection with Plasmodium spp.ResultsLarvae of An. calderoni were found in four localities in 12 out of 244 breeding sites inspected. An. calderoni adults were collected in 14 out of 22 localities during the cross-sectional study and represented 41.3% (459 of 1,111) of the collected adult specimens. Other species found were Anopheles albimanus (54.7%), Anopheles apicimacula (2.1%), Anopheles neivai (1.7%), and Anopheles argyritarsis (0.2%). In the localities that reported the highest malaria Annual Parasite Index (>10/1,000 inhabitants) during the year of sampling, An. calderoni was the predominant species (>90% of the specimens collected). In the longitudinal study, 1,528 An. calderoni were collected by HLC with highest biting rates in February, May and June 2013, periods of high precipitation. In general, the species showed a preference to bite outdoors (p < 0.001). In Boca de Prieta, two specimens of An. calderoni were ELISA positive for Plasmodium circumsporozoite protein: one for P. falciparum and one for Plasmodium vivax VK-210. This represents an overall sporozoite rate of 0.1% and an annual entomological inoculation rate of 2.84 infective bites/human/year.ConclusionsThis study shows that An. calderoni is a primary malaria vector in the southwest of Colombia. Its observed preference for outdoor biting is a major challenge for malaria control.

Project description:Malaria is transmitted by many Anopheles species whose proportionate contributions vary across settings. We re-assessed the roles of Anopheles arabiensis and Anopheles funestus, and examined potential benefits of species-specific interventions in an area in south-eastern Tanzania, where malaria transmission persists, four years after mass distribution of long-lasting insecticide-treated nets (LLINs). Monthly mosquito sampling was done in randomly selected households in three villages using CDC light traps and back-pack aspirators, between January-2015 and January-2016, four years after the last mass distribution of LLINs in 2011. Multiplex polymerase chain reaction (PCR) was used to identify members of An. funestus and Anopheles gambiae complexes. Enzyme-linked immunosorbent assay (ELISA) was used to detect Plasmodium sporozoites in mosquito salivary glands, and to identify sources of mosquito blood meals. WHO susceptibility assays were done on wild caught female An. funestus s.l, and physiological ages approximated by examining mosquito ovaries for parity. A total of 20,135 An. arabiensis and 4,759 An. funestus were collected. The An. funestus group consisted of 76.6% An. funestus s.s, 2.9% An. rivulorum, 7.1% An. leesoni, and 13.4% unamplified samples. Of all mosquitoes positive for Plasmodium, 82.6% were An. funestus s.s, 14.0% were An. arabiensis and 3.4% were An. rivulorum. An. funestus and An. arabiensis contributed 86.21% and 13.79% respectively, of annual entomological inoculation rate (EIR). An. arabiensis fed on humans (73.4%), cattle (22.0%), dogs (3.1%) and chicken (1.5%), but An. funestus fed exclusively on humans. The An. funestus populations were 100% susceptible to organophosphates, pirimiphos methyl and malathion, but resistant to permethrin (10.5% mortality), deltamethrin (18.7%), lambda-cyhalothrin (18.7%) and DDT (26.2%), and had reduced susceptibility to bendiocarb (95%) and propoxur (90.1%). Parity rate was higher in An. funestus (65.8%) than An. arabiensis (44.1%). Though An. arabiensis is still the most abundant vector species here, the remaining malaria transmission is predominantly mediated by An. funestus, possibly due to high insecticide resistance and high survival probabilities. Interventions that effectively target An. funestus mosquitoes could therefore significantly improve control of persistent malaria transmission in south-eastern Tanzania.

Project description:Pyrethroid resistance has been slower to emerge in Anopheles arabiensis than in An. gambiae s.s and An. funestus and, consequently, studies are only just beginning to unravel the genes involved. Permethrin resistance in An. arabiensis in Lower Moshi, Tanzania has been linked to elevated levels of both P450 monooxygenases and ?-esterases. We have conducted a gene expression study to identify specific genes linked with metabolic resistance in the Lower Moshi An. arabiensis population.Microarray experiments employing an An. gambiae whole genome expression chip were performed on An. arabiensis, using interwoven loop designs. Permethrin-exposed survivors were compared to three separate unexposed mosquitoes from the same or a nearby population. A subsection of detoxification genes were chosen for subsequent quantitative real-time PCR (qRT-PCR).Microarray analysis revealed significant over expression of 87 probes and under expression of 85 probes (in pairwise comparisons between permethrin survivors and unexposed sympatric and allopatric samples from Dar es Salaam (controls). For qRT-PCR we targeted over expressed ABC transporter genes (ABC '2060'), a glutathione-S-transferase, P450s and esterases. Design of efficient, specific primers was successful for ABC '2060'and two P450s (CYP6P3, CYP6M2). For the CYP4G16 gene, we used the primers that were previously used in a microarray study of An. arabiensis from Zanzibar islands. Over expression of CYP4G16 and ABC '2060' was detected though with contrasting patterns in pairwise comparisons between survivors and controls. CYP4G16 was only up regulated in survivors, whereas ABC '2060' was similar in survivors and controls but over expressed in Lower Moshi samples compared to the Dar es Salaam samples. Increased transcription of CYP4G16 and ABC '2060' are linked directly and indirectly respectively, with permethrin resistance in Lower Moshi An. arabiensis.Increased transcription of a P450 (CYP4G16) and an ABC transporter (ABC 2060) are linked directly and indirectly respectively, with permethrin resistance in Lower Moshi An. arabiensis. Our study provides replication of CYP4G16 as a candidate gene for pyrethroid resistance in An. arabiensis, although its role may not be in detoxification, and requires further investigation.

Project description:BackgroundGlobally, the Democratic Republic of Congo (DRC) accounted for 9% of malaria cases and 10% of malaria deaths in 2015. As part of control efforts, more than 40 million long-lasting insecticidal nets (LLINs) were distributed between 2008 and 2013, resulting in 70% of households owning one or more LLINs in 2014. To optimize vector control efforts, it is critical to monitor vector behaviour and insecticide resistance trends. Entomological data was collected from eight sentinel sites throughout DRC between 2013 and 2016 in Kingasani, Mikalayi, Lodja, Kabondo, Katana, Kapolowe, Tshikaji and Kalemie. Mosquito species present, relative densities and biting times were monitored using human landing catches (HLC) conducted in eight houses, three times per year. HLC was conducted monthly in Lodja and Kapolowe during 2016 to assess seasonal dynamics. Laboratory data included resistance mechanism frequency and sporozoite rates. Insecticide susceptibility testing was conducted with commonly used insecticides including deltamethrin and permethrin. Synergist bioassays were conducted with PBO to determine the role of oxidases in permethrin resistance.ResultsIn Lodja, monthly Anopheles gambiae s.l. biting rates were consistently high at > 10 bites/person/night indoors and outdoors. In Kapolowe, An. gambiae s.l. dominated during the rainy season, and Anopheles funestus s.l. during the dry season. In all sites, An. gambiae and An. funestus biting occurred mostly late at night. In Kapolowe, significant biting of both species started around 19:00, typically before householders use nets. Sporozoite rates were high, with a mean of 4.3% (95% CI 3.4-5.2) for An. gambiae and 3.3% (95% CI 1.3-5.3) for An. funestus. Anopheles gambiae were resistant to permethrin in six out of seven sites in 2016. In three sites, susceptibility to deltamethrin was observed despite high frequency permethrin resistance, indicating the presence of pyrethroid-specific resistance mechanisms. Pre-exposure to PBO increased absolute permethrin-associated mortality by 24%, indicating that resistance was partly due to metabolic mechanisms. The kdr-1014F mutation in An. gambiae was present at high frequency (> 70%) in three sites (Kabondo, Kingasani and Tshikaji), and lower frequency (< 20%) in two sites (Lodja and Kapolowe).ConclusionThe finding of widespread resistance to permethrin in DRC is concerning and alternative insecticides should be evaluated.

Dataset Information

Linking human behaviours and malaria vector biting risk in south-eastern Tanzania.

Publications

Linking human behaviours and malaria vector biting risk in south-eastern Tanzania.

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