Anopheles drivers of persisting malaria transmission in Guna Yala, Panamá: an operational investigation

Abstract Background Though most of Panamá is free from malaria, localized foci of transmission persist, including in the Guna Yala region. Government-led entomological surveillance using an entomological surveillance planning tool (ESPT) sought to answer programmatically-relevant questions that would enhance the understanding of both local entomological drivers of transmission and gaps in protection that result in persisting malaria transmission to guide local vector control decision-making. Methods The ESPT was used to design a sampling plan centered around the collection of minimum essential indicators to investigate the relevance of LLINs and IRS in the communities of Permé and Puerto Obaldía, Guna Yala, as well as to pinpoint any remaining spaces and times where humans are exposed to Anopheles bites (gaps in protection). Adult Anopheles were collected at three time points via human landing catches (HLCs), CDC Light Traps (LT), and pyrethrum spray catches (PSCs) during the rainy and dry seasons. Mosquitoes were identified to species via molecular methods. Insecticide susceptibility testing of the main vector species to fenitrothion was conducted. Results In total, 7537 adult Anopheles were collected from both sites. Of the 493 specimens molecularly confirmed to species, two thirds (n = 340) were identified as Nyssorhynchus albimanus, followed by Anopheles aquasalis. Overall Anopheles human biting rates (HBRs) were higher outdoors than indoors, and were higher in Permé than in Puerto Obaldía: nightly outdoor HBR ranged from 2.71 bites per person per night (bpn) (Puerto Obaldía), to 221.00 bpn (Permé), whereas indoor nightly HBR ranged from 0.70 bpn (Puerto Obaldía) to 81.90 bpn (Permé). Generally, peak biting occurred during the early evening. The CDC LT trap yields were significantly lower than that of HLCs and this collection method was dropped after the first collection. Pyrethrum spray catches resulted in only three indoor resting Anopheles collected. Insecticide resistance (IR) of Ny. albimanus to fenitrothion was confirmed, with only 65.5% mortality at the diagnostic time. Conclusion The early evening exophagic behaviour of Anopheles vectors, the absence of indoor resting behaviours, and the presence of resistance to the primary intervention insecticide demonstrate limitations of the current malaria strategy, including indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs), and point to both gaps in protection and to the drivers of persisting malaria transmission in Guna Yala. These findings highlight the need for continued and directed entomological surveillance, based on programmatic questions, that generates entomological evidence to inform an adaptive malaria elimination strategy.

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Geographically extensive larval surveys reveal an unexpected scarcity of primary vector mosquitoes in a region of persistent malaria transmission in western Zambia

10.21203/rs.3.rs-43576/v1 ◽

2020 ◽

Author(s):

Dónall Eoin Cross ◽

Chris James Thomas ◽

Niall McKeown ◽

Vincent Siaziyu ◽

Amy Healey ◽

...

Keyword(s):

Malaria Transmission ◽

Nuclear Dna ◽

Indoor Residual Spraying ◽

Genetic Identification ◽

Insecticide Treated Nets ◽

Vector Species ◽

Entomological Surveillance ◽

Wet Season ◽

Genetic Sequencing ◽

Ecological Zones

Abstract Background: The Barotse floodplains of the upper Zambezi River and its tributaries are a highly dynamic environment, with seasonal flooding and transhumance presenting a shifting mosaic of potential larval habitat and human and livestock bloodmeals for malaria vector mosquitoes. However, limited entomological surveillance has been undertaken to characterise the vector community in these floodplains and their environs. Such information is necessary as, despite substantial deployment of insecticide-treated nets (ITNs) and indoor residual spraying (IRS) against Anopheles vectors, malaria transmission persists across Barotseland in Zambia’s Western Province.Methods: Geographically extensive larval surveys were undertaken in two health districts along 102 km of transects, at fine spatial resolution, during a dry season and following the peak of the successive wet season. Larvae were sampled within typical Anopheles flight range of human settlements and identified through genetic sequencing of cytochrome c oxidase I and internal transcribed spacer 2 regions of mitochondrial and nuclear DNA. This facilitated detailed comparison of taxon-specific abundance patterns between ecological zones differentiated by hydrological controls.Results: An unexpected paucity of primary vectors was revealed, with An. gambiae s.l. and An. funestus representing < 2% of 995 sequenced anophelines. Potential secondary vectors predominated in the vector community, primarily An. coustani group species and An. squamosus. Whilst the distribution of An. gambiae s.l. in the study area was highly clustered, secondary vector species were ubiquitous across the landscape in both dry and wet seasons, with some taxon-specific relationships between abundance and ecological zones by season.Conclusions: Larval survey results imply that residual transmission of malaria in Barotseland is being mediated predominantly by secondary vector species, whose known tendencies for crepuscular and outdoor biting renders them largely insensitive to prevalent vector control methods (ITNs and IRS). Alternative interventions may be required against this vector community to further reduce transmission. Larviciding is one potential supplementary intervention, although it presents a challenge in extensive wetlands such as those found in the Upper Zambezi catchment. However, the combination of advances in remote sensing of habitats, genetic identification of local vectors, and spatial modelling present a potential opportunity to optimise targeting of aerial spraying in these environments.

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Heterogeneous Exposure and Hotspots for Malaria Vectors at Three Study Sites in Uganda

10.1101/299529 ◽

2018 ◽

Cited By ~ 1

Author(s):

Su Yun Kang ◽

Katherine E. Battle ◽

Harry S. Gibson ◽

Laura V. Cooper ◽

Kilama Maxwell ◽

...

Keyword(s):

Malaria Transmission ◽

Negative Binomial ◽

Critical Evaluation ◽

Housing Quality ◽

Malaria Vectors ◽

Entomological Surveillance ◽

Malaria Exposure ◽

Dry Seasons ◽

Cold Spots ◽

Study Sites

AbstractHeterogeneity in malaria transmission has household, temporal, and spatial components. These factors are relevant for improving the efficiency of malaria control by targeting heterogeneity. To quantify variation, we analyzed mosquito counts from entomological surveillance conducted at three study sites in Uganda that varied in malaria transmission intensity. Using a Bayesian zero-inflated negative binomial model, validated via a comprehensive simulation study, we quantified household differences in malaria exposure and examined its spatial distribution. We found that housing quality explained large variation among households in mosquito counts. In each site, there was evidence for hot and cold spots, spatial patterns associated with urbanicity, elevation, or other environmental covariates. We also found some differences in the hotspots in rainy vs. dry seasons or before vs. after control. This work identified methods for quantifying heterogeneity in malaria exposure and offered a critical evaluation of spatially targeting interventions at malaria hotspots.

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Efficacy of Actellic 300 CS-based indoor residual spraying on key entomological indicators of malaria transmission in Alibori and Donga, two regions of northern Benin

Parasites & Vectors ◽

10.1186/s13071-019-3865-1 ◽

2019 ◽

Vol 12 (1) ◽

Cited By ~ 1

Author(s):

Albert Sourou Salako ◽

Fortune Dagnon ◽

Arthur Sovi ◽

Gil Germain Padonou ◽

Rock Aïkpon ◽

...

Keyword(s):

Malaria Transmission ◽

Positive Impact ◽

Reduction Rate ◽

Residual Activity ◽

Indoor Residual Spraying ◽

Blood Feeding ◽

Monthly Basis ◽

Human Landing ◽

Parity Rate ◽

Entomological Monitoring

Abstract Background The current study shows the results of three years of IRS entomological monitoring (2016, before intervention; 2017 and 2018, after intervention) performed in Alibori and Donga, northern Benin. Methods Mosquito collections were performed on a monthly basis using human landing catches and pyrethrum spray catches in six districts including four treated with Actellic 300 CS (Kandi, Gogounou, Djougou and Copargo) and two untreated (Bembèrèkè and Kouandé) which served as control sites. Key transmission indicators of Anopheles gambiae (s.l.) as well as the residual activity of Actellic 300 CS assessed through WHO cone tests, were determined. Results The residual efficacy duration of Actellic 300 CS after the two IRS campaigns (2017 and 2018) was 4–5 months (May–September). The parity rate and the sporozoite index of An. gambiae (s.l.) were 36.62% and 0.71%, respectively, after the first spray round in treated areas compared to 57.24% and 3.7%, respectively, in the control areas (P < 0.0001). The same trend was observed after the second spray round. After the first spray round, each person received 1.6 infective bites/month (ib/m) in the treated areas against 12.11 ib/m in the control areas, resulting in a reduction rate of 86.78%. Similarly, the entomological inoculation rate was 1.5 ib/m after the second spray round in the treated areas vs 9.75 ib/m in the control areas, corresponding to a reduction of 84.61%. A decrease in the parity rate (46.26%), sporozoite index (85.75%) and EIR (87.27%) was observed for An. gambiae (s.l.) after the first round of IRS (June–October 2017) compared to the pre-intervention period (June–October 2016). The density of An. gambiae (s.l.) ranged between 0.38–0.48 per house in treated areas vs 1.53–1.76 An. gambiae (s.l.) per house respectively after the first and second IRS rounds. Conclusions This study showed the positive impact of IRS in reducing key entomological parameters of malaria transmission in Alibori and Donga. However, the considerable blood-feeding rate of An. gambiae (s.l.) in spray areas, stress the need for the population to sleep under long-lasting insecticidal nets (LLINs) in addition, to prevent from mosquito bites which did not succeed in resting on sprayed walls.

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Six years of experience in entomological surveillance of indoor residual spraying against malaria transmission in Benin: lessons learned, challenges and outlooks

Malaria Journal ◽

10.1186/s12936-015-0757-5 ◽

2015 ◽

Vol 14 (1) ◽

Cited By ~ 18

Author(s):

Martin C. Akogbéto ◽

Rock Y. Aïkpon ◽

Roseric Azondékon ◽

Gil G. Padonou ◽

Razaki A. Ossè ◽

...

Keyword(s):

Malaria Transmission ◽

Indoor Residual Spraying ◽

Lessons Learned ◽

Years Of Experience ◽

Entomological Surveillance

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Impact of vector control interventions on malaria transmission intensity, outdoor vector biting rates and Anopheles mosquito species composition in Tororo, Uganda

Malaria Journal ◽

10.1186/s12936-019-3076-4 ◽

2019 ◽

Vol 18 (1) ◽

Cited By ~ 10

Author(s):

Alex K. Musiime ◽

David L. Smith ◽

Maxwell Kilama ◽

John Rek ◽

Emmanuel Arinaitwe ◽

...

Keyword(s):

Vector Control ◽

Malaria Transmission ◽

Indoor Residual Spraying ◽

Transmission Intensity ◽

Intervention Period ◽

Malaria Transmission Intensity ◽

Predominant Species ◽

High Transmission ◽

Human Landing ◽

The Impact

Abstract Background Long-lasting insecticidal nets (LLINs) and indoor residual spraying of insecticide (IRS) are widely recommended for the prevention of malaria in endemic regions. Data from human landing catches provide information on the impact of vector control on vector populations. Here, malaria transmission indoors and outdoors, before and after mass deployment of LLINs and IRS in Uganda was compared. Methods The study took place in Tororo district, a historically high transmission area where universal LLIN distribution was conducted in November 2013 and May 2017 and 6 rounds of IRS implemented from December 2014 to July 2018. Human landing catches were performed in 8 houses monthly from October 2011 to September 2012 (pre-intervention period) and every 4 weeks from November 2017 to October 2018 (post-intervention period). Mosquitoes were collected outdoors from 18:00 to 22:00 h and indoors from 18:00 to 06:00 h. Female Anopheles were tested for the presence of Plasmodium falciparum sporozoites and species identification performed using gross dissection and polymerase chain reaction (PCR). Results The interventions were associated with a decline in human biting rate from 19.6 to 2.3 female Anopheles mosquitoes per house per night (p < 0.001) and annual entomological inoculation rate from 129 to 0 infective bites per person per year (p < 0.001). The proportion of mosquitoes collected outdoors increased from 11.6 to 49.4% (p < 0.001). Prior to the interventions the predominant species was Anopheles gambiae sensu stricto (s.s.), which comprised an estimated 76.7% of mosquitoes. Following the interventions, the predominant species was Anopheles arabiensis, which comprised 99.5% of mosquitoes, with almost complete elimination of An. gambiae s.s. (0.5%). Conclusions Mass distribution of LLINs and 6 rounds of IRS dramatically decreased vector density and sporozoite rate resulting in a marked reduction in malaria transmission intensity in a historically high transmission site in Uganda. These changes were accompanied by a shift in vector species from An. gambiae s.s. to An. arabiensis and a relative increase in outdoor biting.

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Geographically extensive larval surveys reveal an unexpected scarcity of primary vector mosquitoes in a region of persistent malaria transmission in western Zambia

10.21203/rs.3.rs-43576/v2 ◽

2020 ◽

Author(s):

Dónall Eoin Cross ◽

Chris James Thomas ◽

Niall McKeown ◽

Vincent Siaziyu ◽

Amy Healey ◽

...

Keyword(s):

Malaria Transmission ◽

Nuclear Dna ◽

Indoor Residual Spraying ◽

Larval Habitat ◽

Insecticide Treated Nets ◽

Vector Species ◽

Entomological Surveillance ◽

Wet Season ◽

Genetic Sequencing ◽

Ecological Zones

Abstract BackgroundThe Barotse floodplains of the upper Zambezi River and its tributaries are a highly dynamic environment, with seasonal flooding and transhumance presenting a shifting mosaic of potential larval habitat and human and livestock bloodmeals for malaria vector mosquitoes. However, limited entomological surveillance has been undertaken to characterise the vector community in these floodplains and their environs. Such information is necessary as, despite substantial deployment of insecticide-treated nets (ITNs) and indoor residual spraying (IRS) against Anopheles vectors, malaria transmission persists across Barotseland in Zambia’s Western Province. MethodsGeographically extensive larval surveys were undertaken in two health districts along 102 km of transects, at fine spatial resolution, during a dry season and following the peak of the successive wet season. Larvae were sampled within typical Anopheles flight range of human settlements and identified through genetic sequencing of cytochrome c oxidase I and internal transcribed spacer 2 regions of mitochondrial and nuclear DNA. This facilitated detailed comparison of taxon-specific abundance patterns between ecological zones differentiated by hydrological controls.ResultsAn unexpected paucity of primary vectors was revealed, with An. gambiae s.l. and An. funestus representing <2% of 995 sequenced anophelines. Potential secondary vectors predominated in the vector community, primarily An. coustani group species and An squamosus. Whilst the distribution of An. gambiae s.l. in the study area was highly clustered, secondary vector species were ubiquitous across the landscape in both dry and wet seasons, with some taxon-specific relationships between abundance and ecological zones by season.ConclusionsThe diversity of candidate vector species and their high relative abundance observed across diverse hydro-ecosystems indicates a highly adaptable transmission system, resilient to environmental variation and, potentially, interventions that target only part of the vector community. Larval survey results imply that residual transmission of malaria in Barotseland is being mediated predominantly by secondary vector species, whose known tendencies for crepuscular and outdoor biting renders them largely insensitive to prevalent vector control methods.

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Geographically extensive larval surveys reveal an unexpected scarcity of primary vector mosquitoes in a region of persistent malaria transmission in western Zambia

10.21203/rs.3.rs-43576/v3 ◽

2020 ◽

Author(s):

Dónall Eoin Cross ◽

Chris James Thomas ◽

Niall McKeown ◽

Vincent Siaziyu ◽

Amy Healey ◽

...

Keyword(s):

Malaria Transmission ◽

Nuclear Dna ◽

Indoor Residual Spraying ◽

Larval Habitat ◽

Insecticide Treated Nets ◽

Vector Species ◽

Entomological Surveillance ◽

Wet Season ◽

Genetic Sequencing ◽

Ecological Zones

Abstract BackgroundThe Barotse floodplains of the upper Zambezi River and its tributaries are a highly dynamic environment, with seasonal flooding and transhumance presenting a shifting mosaic of potential larval habitat and human and livestock bloodmeals for malaria vector mosquitoes. However, limited entomological surveillance has been undertaken to characterise the vector community in these floodplains and their environs. Such information is necessary as, despite substantial deployment of insecticide-treated nets (ITNs) and indoor residual spraying (IRS) against Anopheles vectors, malaria transmission persists across Barotseland in Zambia’s Western Province. MethodsGeographically extensive larval surveys were undertaken in two health districts along 102 km of transects, at fine spatial resolution, during a dry season and following the peak of the successive wet season. Larvae were sampled within typical Anopheles flight range of human settlements and identified through genetic sequencing of cytochrome c oxidase I and internal transcribed spacer 2 regions of mitochondrial and nuclear DNA. This facilitated detailed comparison of taxon-specific abundance patterns between ecological zones differentiated by hydrological controls.ResultsAn unexpected paucity of primary vectors was revealed, with An. gambiae s.l. and An. funestus representing <2% of 995 sequenced anophelines. Potential secondary vectors predominated in the vector community, primarily An. coustani group species and An squamosus. Whilst the distribution of An. gambiae s.l. in the study area was highly clustered, secondary vector species were ubiquitous across the landscape in both dry and wet seasons, with some taxon-specific relationships between abundance and ecological zones by season. ConclusionsThe diversity of candidate vector species and their high relative abundance observed across diverse hydro-ecosystems indicates a highly adaptable transmission system, resilient to environmental variation and, potentially, interventions that target only part of the vector community. Larval survey results imply that residual transmission of malaria in Barotseland is being mediated predominantly by secondary vector species, whose known tendencies for crepuscular and outdoor biting renders them largely insensitive to prevalent vector control methods.

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Upsurge of malaria transmission after indoor residual spraying withdrawal in Atacora region in Benin, West Africa

Malaria Journal ◽

10.1186/s12936-019-3086-2 ◽

2020 ◽

Vol 19 (1) ◽

Author(s):

Rock Yves Aïkpon ◽

Gil Padonou ◽

Fortuné Dagnon ◽

Razaki Ossè ◽

Aurore Ogouyemi Hounto ◽

...

Keyword(s):

Malaria Transmission ◽

Indoor Residual Spraying ◽

Bed Nets ◽

Malaria Vector Control ◽

Chain Reaction ◽

Molecular Species Identification ◽

Vector Abundance ◽

Human Landing ◽

Drastic Increase ◽

Polymerase Chain

Abstract Background In Benin, malaria vector control mostly relies on long-lasting, insecticidal-treated bed nets (LLINs) and indoor residual spraying (IRS) operations. From 2011 to 2016, an IRS programme has been implemented in Atacora region. However, in 2017 the programme was withdrawn from two other regions in the northern part of the country, with hopes that gains would be relatively sustained because of the seasonality of malaria transmission. What would be the vulnerability of populations to malaria after the withdrawal of IRS? Methods Monthly mosquito collections were performed through human landing captures (HLCs) for 24 months (from January to December 2016 during the last IRS campaign, and from January to December 2018, 2 years after the withdrawal of IRS). Vector mosquitoes biting density was sampled by HLC and was tested for presence of Plasmodium falciparum sporozoites. The carcass of these mosquitoes (abdomens, wing, legs) were subjected to molecular species identification using polymerase chain reaction (PCR) assays. Results It is noticed a drastic increase (~ 3 times higher) of vector abundance after the withdrawal of IRS. Mosquito biting rates in the 3 survey districts increased significantly after IRS was withdrawn. In 2018, after IRS cessation a significant increase of entomological inoculation rate was recorded, where each inhabitant received an average of 94.9 infected bites/year to 129.21 infected bites/year against an average of 17.15 infected bites/year to 24.82 infected bites/year in 2016. Conclusion It is obvious that the withdrawal of IRS confers a vulnerability of the population with regard to the malaria transmission. Robust monitoring is needed to better understand when and where IRS should be most adequate, or can be safely withdrawn. In case of withdrawal, adapted accompanying measures should be proposed according to the context not only to maintain the gains capitalized with IRS, but also to avoid any rebound of transmission.

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Geographically extensive larval surveys reveal an unexpected scarcity of primary vector mosquitoes in a region of persistent malaria transmission in western Zambia

Parasites & Vectors ◽

10.1186/s13071-020-04540-1 ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Dónall Eoin Cross ◽

Chris Thomas ◽

Niall McKeown ◽

Vincent Siaziyu ◽

Amy Healey ◽

...

Keyword(s):

Malaria Transmission ◽

Nuclear Dna ◽

Indoor Residual Spraying ◽

Larval Habitat ◽

Insecticide Treated Nets ◽

Vector Species ◽

Entomological Surveillance ◽

Wet Season ◽

Genetic Sequencing ◽

Ecological Zones

Abstract Background The Barotse floodplains of the upper Zambezi River and its tributaries are a highly dynamic environment, with seasonal flooding and transhumance presenting a shifting mosaic of potential larval habitat and human and livestock blood meals for malaria vector mosquitoes. However, limited entomological surveillance has been undertaken to characterize the vector community in these floodplains and their environs. Such information is necessary as, despite substantial deployment of insecticide-treated nets (ITNs) and indoor residual spraying (IRS) against Anopheles vectors, malaria transmission persists across Barotseland in Zambia’s Western Province. Methods Geographically extensive larval surveys were undertaken in two health districts along 102 km of transects, at fine spatial resolution, during a dry season and following the peak of the successive wet season. Larvae were sampled within typical Anopheles flight range of human settlements and identified through genetic sequencing of cytochrome c oxidase I and internal transcribed spacer two regions of mitochondrial and nuclear DNA. This facilitated detailed comparison of taxon-specific abundance patterns between ecological zones differentiated by hydrological controls. Results An unexpected paucity of primary vectors was revealed, with An. gambiae s.l. and An. funestus representing < 2% of 995 sequenced anophelines. Potential secondary vectors predominated in the vector community, primarily An. coustani group species and An. squamosus. While the distribution of An. gambiae s.l. in the study area was highly clustered, secondary vector species were ubiquitous across the landscape in both dry and wet seasons, with some taxon-specific relationships between abundance and ecological zones by season. Conclusions The diversity of candidate vector species and their high relative abundance observed across diverse hydro-ecosystems indicate a highly adaptable transmission system, resilient to environmental variation and, potentially, interventions that target only part of the vector community. Larval survey results imply that residual transmission of malaria in Barotseland is being mediated predominantly by secondary vector species, whose known tendencies for crepuscular and outdoor biting renders them largely insensitive to prevalent vector control methods.

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