Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia

Understanding the genetic diversity and transmission dynamics of Plasmodium falciparum, the causative agent of malaria, is crucial for effective control and elimination efforts. In some endemic regions, malaria is highly seasonal with no or little transmission during up to 8 mo, yet little is known...

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Main Authors: Marc-Antoine Guery, Sukai Ceesay, Sainabou Drammeh, Fatou K Jaiteh, Umberto D'Alessandro, Teun Bousema, David J Conway, Antoine Claessens
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-05-01
Series:eLife
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Online Access:https://elifesciences.org/articles/103047
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author Marc-Antoine Guery
Sukai Ceesay
Sainabou Drammeh
Fatou K Jaiteh
Umberto D'Alessandro
Teun Bousema
David J Conway
Antoine Claessens
author_facet Marc-Antoine Guery
Sukai Ceesay
Sainabou Drammeh
Fatou K Jaiteh
Umberto D'Alessandro
Teun Bousema
David J Conway
Antoine Claessens
author_sort Marc-Antoine Guery
collection DOAJ
description Understanding the genetic diversity and transmission dynamics of Plasmodium falciparum, the causative agent of malaria, is crucial for effective control and elimination efforts. In some endemic regions, malaria is highly seasonal with no or little transmission during up to 8 mo, yet little is known about how seasonality affects the parasite population genetics. Here, we conducted a longitudinal study over 2.5 y on 1516 participants in the Upper River Region of The Gambia. With 425 P. falciparum genetic barcodes genotyped from asymptomatic infections, we developed an identity by descent (IBD) based pipeline and validated its accuracy against 199 parasite genomes sequenced from the same isolates. Genetic relatedness between isolates revealed a very low inbreeding level, suggesting continuous recombination among parasites rather than the dominance of specific strains. However, isolates from the same household were sixfold more likely to be genetically related compared to those from other villages, suggesting close transmission links within households. Seasonal variation also influenced parasite genetics, with most differentiation occurring during the transition from the low transmission season to the subsequent high transmission season. Yet chronic infections presented exceptions, including one individual who had a continuous infection by the same parasite genotype for at least 18 mo. Our findings highlight the burden of asymptomatic chronic malaria carriers and the importance of characterizing the parasite genetic population at the community-level. Most importantly, ‘reactive’ approaches for malaria elimination should not be limited to acute malaria cases but be broadened to households of asymptomatic carriers.
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spelling doaj-art-3cfe1c9817fd43a88fafe6b4948c96b62025-08-20T03:47:58ZengeLife Sciences Publications LtdeLife2050-084X2025-05-011310.7554/eLife.103047Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The GambiaMarc-Antoine Guery0Sukai Ceesay1Sainabou Drammeh2Fatou K Jaiteh3Umberto D'Alessandro4https://orcid.org/0000-0001-6341-5009Teun Bousema5https://orcid.org/0000-0003-2666-094XDavid J Conway6Antoine Claessens7https://orcid.org/0000-0002-4277-0914LPHI, MIVEGEC, University of Montpellier, CNRS, INSERM, Montpellier, FranceMedical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, GambiaMedical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, GambiaMedical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, GambiaMedical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, GambiaRadboud University Medical Center, Radboud Institute for Health Sciences, Department of Medical Microbiology, Nijmegen, NetherlandsDepartment of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomLPHI, MIVEGEC, University of Montpellier, CNRS, INSERM, Montpellier, France; Medical Research Council Unit The Gambia at the London School of Hygiene and Tropical Medicine, Banjul, Gambia; Department of Infection Biology, London School of Hygiene and Tropical Medicine, London, United KingdomUnderstanding the genetic diversity and transmission dynamics of Plasmodium falciparum, the causative agent of malaria, is crucial for effective control and elimination efforts. In some endemic regions, malaria is highly seasonal with no or little transmission during up to 8 mo, yet little is known about how seasonality affects the parasite population genetics. Here, we conducted a longitudinal study over 2.5 y on 1516 participants in the Upper River Region of The Gambia. With 425 P. falciparum genetic barcodes genotyped from asymptomatic infections, we developed an identity by descent (IBD) based pipeline and validated its accuracy against 199 parasite genomes sequenced from the same isolates. Genetic relatedness between isolates revealed a very low inbreeding level, suggesting continuous recombination among parasites rather than the dominance of specific strains. However, isolates from the same household were sixfold more likely to be genetically related compared to those from other villages, suggesting close transmission links within households. Seasonal variation also influenced parasite genetics, with most differentiation occurring during the transition from the low transmission season to the subsequent high transmission season. Yet chronic infections presented exceptions, including one individual who had a continuous infection by the same parasite genotype for at least 18 mo. Our findings highlight the burden of asymptomatic chronic malaria carriers and the importance of characterizing the parasite genetic population at the community-level. Most importantly, ‘reactive’ approaches for malaria elimination should not be limited to acute malaria cases but be broadened to households of asymptomatic carriers.https://elifesciences.org/articles/103047Malariagenomeepidemiology
spellingShingle Marc-Antoine Guery
Sukai Ceesay
Sainabou Drammeh
Fatou K Jaiteh
Umberto D'Alessandro
Teun Bousema
David J Conway
Antoine Claessens
Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
eLife
Malaria
genome
epidemiology
title Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
title_full Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
title_fullStr Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
title_full_unstemmed Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
title_short Household clustering and seasonal genetic variation of Plasmodium falciparum at the community-level in The Gambia
title_sort household clustering and seasonal genetic variation of plasmodium falciparum at the community level in the gambia
topic Malaria
genome
epidemiology
url https://elifesciences.org/articles/103047
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