Infection length and host environment influence on Plasmodium falciparum dry season reservoir
(2024) In EMBO Molecular Medicine 16(10). p.2349-2375- 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... (More)
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.
(Less)
- author
- organization
- publishing date
- 2024-10-14
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Asymptomatic, Dry Season, Infection Length, Malaria, Sensing
- in
- EMBO Molecular Medicine
- volume
- 16
- issue
- 10
- pages
- 27 pages
- publisher
- Wiley-Blackwell
- external identifiers
-
- pmid:39284949
- scopus:85203959162
- ISSN
- 1757-4676
- DOI
- 10.1038/s44321-024-00127-w
- language
- English
- LU publication?
- yes
- additional info
- Publisher Copyright: © The Author(s) 2024.
- id
- 713b0723-2d6c-4999-86cc-735249d6db67
- date added to LUP
- 2024-12-04 11:29:38
- date last changed
- 2025-07-03 05:18:11
@article{713b0723-2d6c-4999-86cc-735249d6db67,
abstract = {{<p>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.</p>}},
author = {{Andrade, Carolina M. and Carrasquilla, Manuela and Dabbas, Usama and Briggs, Jessica and van Dijk, Hannah and Sergeev, Nikolay and Sissoko, Awa and Niangaly, Moussa and Ntalla, Christina and LaVerriere, Emily and Skinner, Jeff and Golob, Klara and Richter, Jeremy and Cisse, Hamidou and Li, Shanping and Hendry, Jason A. and Asghar, Muhammad and Doumtabe, Didier and Farnert, Anna and Ruppert, Thomas and Neafsey, Daniel E. and Kayentao, Kassoum and Doumbo, Safiatou and Ongoiba, Aissata and Crompton, Peter D. and Traore, Boubacar and Greenhouse, Bryan and Portugal, Silvia}},
issn = {{1757-4676}},
keywords = {{Asymptomatic; Dry Season; Infection Length; Malaria; Sensing}},
language = {{eng}},
month = {{10}},
number = {{10}},
pages = {{2349--2375}},
publisher = {{Wiley-Blackwell}},
series = {{EMBO Molecular Medicine}},
title = {{Infection length and host environment influence on Plasmodium falciparum dry season reservoir}},
url = {{http://dx.doi.org/10.1038/s44321-024-00127-w}},
doi = {{10.1038/s44321-024-00127-w}},
volume = {{16}},
year = {{2024}},
}