Infection length and host environment influence on Plasmodium falciparum dry season reservoir

Persistence of malaria parasites in asymptomatic hosts is crucial in areas of seasonally-interrupted transmission, where P. falciparum bridges wet seasons months apart. During the dry season, infected erythrocytes exhibit extended circulation with reduced cytoadherence, increasing the risk of splenic clearance of infected cells and hindering parasitaemia increase. However, what determines parasite persistence for long periods of time remains unknown. Here, we investigated whether seasonality affects plasma composition so that P. falciparum can detect and adjust to changing serological cues; or if alternatively, parasite infection length dictates clinical presentation and persistency. Data from Malian children exposed to alternating ~6-month wet and dry seasons show that plasma composition is unrelated to time of year in non-infected children, and that carrying P. falciparum only minimally affects plasma constitution in asymptomatic hosts. Parasites persisting in the blood of asymptomatic children from the dry into the ensuing wet season rarely if ever appeared to cause malaria in their hosts as seasons changed. In vitro culture in the presence of plasma collected in the dry or the wet seasons did not affect parasite development, replication or host-cell remodelling. The absence of a parasite-encoded sensing mechanism was further supported by the observation of similar features in P. falciparum persisting asymptomatically in the dry season and parasites in age- and sex-matched asymptomatic children in the wet season. Conversely, we show that P. falciparum clones transmitted early in the wet season had lower chance of surviving until the end of the following dry season, contrasting with a higher likelihood of survival of clones transmitted towards the end of the wet season, allowing for the re-initiation of transmission. We propose that the decreased virulence observed in persisting parasites during the dry season is not due to the parasites sensing ability, nor is it linked to a decreased capacity for parasite replication but rather a consequence decreased cytoadhesion associated with infection length.

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Publication Details

Journal
EMBO Molecular Medicine
Published
2024-09-16
DOI
https://doi.org/10.1038/s44321-024-00127-w
Citations
11
Primary Topic
Malaria Research and Control
Type
article
Field-Weighted Citation Impact
5.43

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article

Infection length and host environment influence on Plasmodium falciparum dry season reservoir

Jason A. Hendry, Hannah van Dijk, Shanping Li, Nikolay Sergeev et al.
11 citations
EMBO Molecular Medicine
Malaria Research and Control
5.43
article

Infection length and host environment influence on Plasmodium falciparum dry season reservoir

Jason A. Hendry, Hannah van Dijk, Shanping Li, Nikolay Sergeev, Jessica Briggs, Sílvia Portugal, Kassoum Kayentao, Aïssata Ongoïba, Manuela Carrasquilla, Boubacar Traoré, Thomas Ruppert, Hamidou Cisse, Anna Färnert, Carolina M. Andrade, Peter D. Crompton, Usama Dabbas, Safiatou Doumbo, Bryan Greenhouse, Emily LaVerriere, Daniel E. Neafsey, Moussa Niangaly, Muhammad Asghar, Jeff Skinner, Christina Ntalla, Klara Golob, Didier Doumtabe, Awa Sissoko, Jeremy Richter
article en
11 citations

Abstract

Persistence of malaria parasites in asymptomatic hosts is crucial in areas of seasonally-interrupted transmission, where P. falciparum bridges wet seasons months apart. During the dry season, infected erythrocytes exhibit extended circulation with reduced cytoadherence, increasing the risk of splenic clearance of infected cells and hindering parasitaemia increase. However, what determines parasite persistence for long periods of time remains unknown. Here, we investigated whether seasonality affects plasma composition so that P. falciparum can detect and adjust to changing serological cues; or if alternatively, parasite infection length dictates clinical presentation and persistency. Data from Malian children exposed to alternating ~6-month wet and dry seasons show that plasma composition is unrelated to time of year in non-infected children, and that carrying P. falciparum only minimally affects plasma constitution in asymptomatic hosts. Parasites persisting in the blood of asymptomatic children from the dry into the ensuing wet season rarely if ever appeared to cause malaria in their hosts as seasons changed. In vitro culture in the presence of plasma collected in the dry or the wet seasons did not affect parasite development, replication or host-cell remodelling. The absence of a parasite-encoded sensing mechanism was further supported by the observation of similar features in P. falciparum persisting asymptomatically in the dry season and parasites in age- and sex-matched asymptomatic children in the wet season. Conversely, we show that P. falciparum clones transmitted early in the wet season had lower chance of surviving until the end of the following dry season, contrasting with a higher likelihood of survival of clones transmitted towards the end of the wet season, allowing for the re-initiation of transmission. We propose that the decreased virulence observed in persisting parasites during the dry season is not due to the parasites sensing ability, nor is it linked to a decreased capacity for parasite replication but rather a consequence decreased cytoadhesion associated with infection length.

EMBO Molecular MedicineVol. 16(10)
Broad Institute (US), San Francisco General Hospital (US), National Institutes of Health (US), Karolinska University Hospital (SE), Harvard University (US), Radboud University Nijmegen (NL), University of California, San Francisco (US), Lund University (SE), Heidelberg University (DE), University Hospital Heidelberg (DE), Radboud University Medical Center (NL), Heidelberg University of Education (DE), Max Planck Institute for Infection Biology (DE), Radboud Institute for Molecular Life Sciences (NL), Université des Sciences, des Techniques et des Technologies de Bamako (ML), Chan Zuckerberg Initiative (United States) (US), Heidelberg Engineering (Germany) (DE), Max Planck Institute for the History of Science (DE), National University of Sciences and Technology (PK)
Division of Intramural Research, National Institute of Allergy and Infectious Diseases, Deutsches Zentrum für Infektionsforschung, European Commission, Max-Planck-Gesellschaft, National Institutes of Health, National Institute of Allergy and Infectious Diseases, Division of Microbiology and Infectious Diseases, National Institute of Allergy and Infectious Diseases, NHLBI Division of Intramural Research, HORIZON EUROPE European Research Council
Openalex Percentile: Top 4%
Malaria Research and Control
5.43
DOIOpen Access PDFOpenAlex
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