The impact of indoor residual spraying on <i>Plasmodium falciparum</i> microsatellite variation in an area of high seasonal malaria transmission in Ghana, West Africa

Argyropoulos, Dionne C.; Ruybal‐Pesántez, Shazia; Deed, Samantha; Oduro, Abraham; Dadzie, Samuel; Appawu, Maxwell A.; Asoala, Victor; Pascual, Mercedes; Koram, Kwadwo A.; Day, Karen P.; Tiedje, Kathryn E.

doi:10.1111/mec.16029

Cited by 8 publications

(13 citation statements)

References 99 publications

(158 reference statements)

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“…Of the remaining monoclonal samples that were able to be analysed, our results from SNP barcodes did not reflect diversity, similarity and structure estimates as found in other studies using a higher magnitude of genome-wide SNPs ( Mobegi et al, 2014 ; Daniels et al, 2015 ; Amambua-Ngwa et al, 2019 ; Moser et al, 2020 ; Verity et al, 2020 ; MalariaGEN et al, 2021 ), putatively neutral microsatellites ( Anderson et al, 2000 ; Mobegi et al, 2012 ; Duffy et al, 2017 ; Argyropoulos et al, 2021 ) and antigenic markers ( Ruybal-Pesántez et al, 2017b ; Day et al, 2017 ; Rorick et al, 2018 ). One possible explanation for these observed discrepancies is the “ascertainment bias” phenomenon, where polymorphisms that were discovered in few samples or locations can result in a deviation from an expected allele frequency distribution ( Kuhner et al, 2000 ; Wakeley et al, 2001 ; Helyar et al, 2011 ).…”

Section: Discussioncontrasting

confidence: 67%

“…The answer likely lies in the use of polymorphic markers such as putatively neutral markers that permit the inclusion of “dominant” infections (e.g., short tandem repeats (STRs) or microsatellites) ( Anderson et al, 1999 ; Tessema et al, 2020 ). For example, microsatellites were able to resolve global P. falciparum structure with only 12 markers ( Anderson et al, 2000 ), while 9-10 microsatellite markers were able to give realistic assessments of these measures related to both long-lasting insecticidal net (LLIN) ( Kattenberg et al, 2019 ) and indoor residual spraying (IRS) ( Argyropoulos et al, 2021 ) interventions, respectively, in moderate-to-high transmission settings. With respect to neutral variation, STR loci are more useful to detect recent population expansions than SNPs as they accumulate new mutations at a faster rate, are multiallelic often in excess of 10 alleles, and have more private alleles; thus they remain the most informative putatively neutral markers in population genetic studies across many organisms ( Ellegren, 2004 ; Selkoe and Toonen, 2006 ; Guichoux et al, 2011 ), including in P. falciparum and P. vivax genomes across various geographic populations ( Han et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

“…To identify finer-scale levels of structure without geospatial location data for each individual isolate, we calculated the pairwise allele sharing ( P AS ) score for isolates within each study population for each barcode using the “complete monoclonal infections” haplotypes with no missing data. P AS is an identity-by-state (IBS) measure of genetic similarity that can be used across relatively few loci and was calculated as the number of alleles shared between two multilocus haplotypes ( N AB ) divided by the number of SNP loci ( N L ) ( P AS = N AB / N L ) ( Ruybal-Pesántez et al, 2017a ; Argyropoulos et al, 2021 ). The P AS score characterised variation in multilocus haplotypes from clones ( P AS = 1.0) to genetically dissimilar ( P AS ≤ 0.25) ( Argyropoulos et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

“…P AS is an identity-by-state (IBS) measure of genetic similarity that can be used across relatively few loci and was calculated as the number of alleles shared between two multilocus haplotypes ( N AB ) divided by the number of SNP loci ( N L ) ( P AS = N AB / N L ) ( Ruybal-Pesántez et al, 2017a ; Argyropoulos et al, 2021 ). The P AS score characterised variation in multilocus haplotypes from clones ( P AS = 1.0) to genetically dissimilar ( P AS ≤ 0.25) ( Argyropoulos et al, 2021 ). Larger-scale genomic measures like identity-by-descent (IBD) are performed for larger genome sequences (a minimum of 200 biallelic loci) to infer similarity or “relatedness” over a range of DNA segments ( Henden et al, 2018 ; Schaffner et al, 2018 ; Taylor et al, 2019 ) and therefore were unable to be pursued.…”

Section: Methodsmentioning

confidence: 99%

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Performance of SNP barcodes to determine genetic diversity and population structure of Plasmodium falciparum in Africa

et al. 2023

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Panels of informative biallelic single nucleotide polymorphisms (SNPs) have been proposed to be an economical method to fast-track the population genetic analysis of Plasmodium falciparum in malaria-endemic areas. Whilst used successfully in low-transmission areas where infections are monoclonal and highly related, we present the first study to evaluate the performance of these 24- and 96-SNP molecular barcodes in African countries, characterised by moderate-to-high transmission, where multiclonal infections are prevalent. For SNP barcodes it is generally recommended that the SNPs chosen i) are biallelic, ii) have a minor allele frequency greater than 0.10, and iii) are independently segregating, to minimise bias in the analysis of genetic diversity and population structure. Further, to be standardised and used in many population genetic studies, these barcodes should maintain characteristics i) to iii) across various iv) geographies and v) time points. Using haplotypes generated from the MalariaGEN P. falciparum Community Project version six database, we investigated the ability of these two barcodes to fulfil these criteria in moderate-to-high transmission African populations in 25 sites across 10 countries. Predominantly clinical infections were analysed, with 52.3% found to be multiclonal, generating high proportions of mixed-allele calls (MACs) per isolate thereby impeding haplotype construction. Of the 24- and 96-SNPs, loci were removed if they were not biallelic and had low minor allele frequencies in all study populations, resulting in 20- and 75-SNP barcodes respectively for downstream population genetics analysis. Both SNP barcodes had low expected heterozygosity estimates in these African settings and consequently biased analyses of similarity. Both minor and major allele frequencies were temporally unstable. These SNP barcodes were also shown to identify weak genetic differentiation across large geographic distances based on Mantel Test and DAPC. These results demonstrate that these SNP barcodes are vulnerable to ascertainment bias and as such cannot be used as a standardised approach for malaria surveillance in moderate-to-high transmission areas in Africa, where the greatest genomic diversity of P. falciparum exists at local, regional and country levels.

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Section: Discussioncontrasting

confidence: 67%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Performance of SNP barcodes to determine genetic diversity and population structure of Plasmodium falciparum in Africa

et al. 2023

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“…Plasmodium falciparum genetic data can complement existing epidemiological surveillance strategies to inform transmission dynamics and patterns. For example, malaria genomics has been used to understand changes in transmission intensity (1) including following the implementation of interventions (2)(3)(4), to monitor the emergence and spread of drug (5)(6)(7) and diagnostic resistance (8,9), and to identify patterns of connectivity between parasite populations impacting control efforts (10)(11)(12)(13). Aside from genomic applications associated with phenotypic signatures in the parasite populations, such as drug or diagnostic resistance, many applications of malaria genomics rely on identifying levels of parasite relatedness (14,15).…”

Section: Introductionmentioning

confidence: 99%

Exploring how space, time, and sampling impact our ability to measure genetic structure across Plasmodium falciparum populations

Arambepola

Bérubé²,

Freedman³

et al. 2023

Front. Epidemiol.

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A primary use of malaria parasite genomics is identifying highly related infections to quantify epidemiological, spatial, or temporal factors associated with patterns of transmission. For example, spatial clustering of highly related parasites can indicate foci of transmission and temporal differences in relatedness can serve as evidence for changes in transmission over time. However, for infections in settings of moderate to high endemicity, understanding patterns of relatedness is compromised by complex infections, overall high forces of infection, and a highly diverse parasite population. It is not clear how much these factors limit the utility of using genomic data to better understand transmission in these settings. In particular, further investigation is required to determine which patterns of relatedness we expect to see with high quality, densely sampled genomic data in a high transmission setting and how these observations change under different study designs, missingness, and biases in sample collection. Here we investigate two identity-by-state measures of relatedness and apply them to amplicon deep sequencing data collected as part of a longitudinal cohort in Western Kenya that has previously been analysed to identify individual-factors associated with sharing parasites with infected mosquitoes. With these data we use permutation tests, to evaluate several hypotheses about spatiotemporal patterns of relatedness compared to a null distribution. We observe evidence of temporal structure, but not of fine-scale spatial structure in the cohort data. To explore factors associated with the lack of spatial structure in these data, we construct a series of simplified simulation scenarios using an agent based model calibrated to entomological, epidemiological and genomic data from this cohort study to investigate whether the lack of spatial structure observed in the cohort could be due to inherent power limitations of this analytical method. We further investigate how our hypothesis testing behaves under different sampling schemes, levels of completely random and systematic missingness, and different transmission intensities.

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Indoor residual spraying for preventing malaria in communities using insecticide-treated nets

Pryce

Medley

Choi

2022

Cochrane Database of Systematic Reviews

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Background Insecticide‐treated nets (ITNs) and indoor residual spraying (IRS) are used to prevent malaria transmission. Both interventions use insecticides to kill mosquitoes that bite and rest indoors. Adding IRS to ITNs may improve malaria control simply because two interventions can be better than one. Furthermore, IRS may improve malaria control where ITNs are failing due to insecticide resistance. Pyrethroid insecticides are the predominant class of insecticide used for ITNs, as they are more safe than other insecticide classes when in prolonged contact with human skin. While many mosquito populations have developed some resistance to pyrethroid insecticides, a wider range of insecticides can be used for IRS. This review is an update of the previous Cochrane 2019 edition. Objectives To summarize the effect on malaria of additionally implementing IRS, using non‐pyrethroid‐like or pyrethroid‐like insecticides, in communities currently using ITNs. Search methods We searched the Cochrane Infectious Diseases Group Specialized Register; CENTRAL; MEDLINE; and five other databases for records from 1 January 2000 to 8 November 2021, on the basis that ITN programmes did not begin to be implemented as policy before the year 2000. Selection criteria We included cluster‐randomized controlled trials (cRCTs), interrupted time series (ITS), or controlled before‐after studies (CBAs) comparing IRS plus ITNs with ITNs alone. We included studies with at least 50% ITN ownership (defined as the proportion of households owning one or more ITN) in both study arms. Data collection and analysis Two review authors independently assessed studies for eligibility, analyzed risk of bias, and extracted data. We used risk ratio (RR) and 95% confidence intervals (CI). We stratified by type of insecticide, 'pyrethroid‐like' and 'non‐pyrethroid‐like'; the latter could improve malaria control better than adding IRS insecticides that have the same way of working as the insecticide on ITNs ('pyrethroid‐like'). We used subgroup analysis of ITN usage in the studies to explore heterogeneity. We assessed the certainty of evidence using the GRADE approach. Main results Eight cRCTs (10 comparisons), one CBA, and one ITS study, all conducted since 2008 in sub‐Saharan Africa, met our inclusion criteria. The primary vectors in all sites were mosquitoes belonging to the Anopheles gambiae s.l. complex species; five studies in Benin, Mozambique, Ghana, Sudan, and Tanzania also reported the vector Anopheles funestus . Five cRCTs and both quasi‐experimental design studies used insecticides with targets different to pyrethroids (two used bendiocarb, three used pirimiphos‐methyl, and one used propoxur. Each of these studies were conducted in areas where the vectors were described as resistant or highly resistant to pyrethroids. Two...

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The impact of indoor residual spraying on Plasmodium falciparum microsatellite variation in an area of high seasonal malaria transmission in Ghana, West Africa

Cited by 8 publications

References 99 publications

Performance of SNP barcodes to determine genetic diversity and population structure of Plasmodium falciparum in Africa

Performance of SNP barcodes to determine genetic diversity and population structure of Plasmodium falciparum in Africa

Exploring how space, time, and sampling impact our ability to measure genetic structure across Plasmodium falciparum populations

Indoor residual spraying for preventing malaria in communities using insecticide-treated nets

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