Infection length and host environment influence on Plasmodium falciparum dry season reservoir
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...
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Springer Nature
2024-09-01
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| Online Access: | https://doi.org/10.1038/s44321-024-00127-w |
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| author | Carolina M Andrade Manuela Carrasquilla Usama Dabbas Jessica Briggs Hannah van Dijk Nikolay Sergeev Awa Sissoko Moussa Niangaly Christina Ntalla Emily LaVerriere Jeff Skinner Klara Golob Jeremy Richter Hamidou Cisse Shanping Li Jason A Hendry Muhammad Asghar Didier Doumtabe Anna Farnert Thomas Ruppert Daniel E Neafsey Kassoum Kayentao Safiatou Doumbo Aissata Ongoiba Peter D Crompton Boubacar Traore Bryan Greenhouse Silvia Portugal |
| author_facet | Carolina M Andrade Manuela Carrasquilla Usama Dabbas Jessica Briggs Hannah van Dijk Nikolay Sergeev Awa Sissoko Moussa Niangaly Christina Ntalla Emily LaVerriere Jeff Skinner Klara Golob Jeremy Richter Hamidou Cisse Shanping Li Jason A Hendry Muhammad Asghar Didier Doumtabe Anna Farnert Thomas Ruppert Daniel E Neafsey Kassoum Kayentao Safiatou Doumbo Aissata Ongoiba Peter D Crompton Boubacar Traore Bryan Greenhouse Silvia Portugal |
| author_sort | Carolina M Andrade |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-9b3ff732567a4f43bf41822cfe3ec2fd |
| institution | OA Journals |
| issn | 1757-4684 |
| language | English |
| publishDate | 2024-09-01 |
| publisher | Springer Nature |
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| series | EMBO Molecular Medicine |
| spelling | doaj-art-9b3ff732567a4f43bf41822cfe3ec2fd2025-08-20T02:17:46ZengSpringer NatureEMBO Molecular Medicine1757-46842024-09-0116102349237510.1038/s44321-024-00127-wInfection length and host environment influence on Plasmodium falciparum dry season reservoirCarolina M Andrade0Manuela Carrasquilla1Usama Dabbas2Jessica Briggs3Hannah van Dijk4Nikolay Sergeev5Awa Sissoko6Moussa Niangaly7Christina Ntalla8Emily LaVerriere9Jeff Skinner10Klara Golob11Jeremy Richter12Hamidou Cisse13Shanping Li14Jason A Hendry15Muhammad Asghar16Didier Doumtabe17Anna Farnert18Thomas Ruppert19Daniel E Neafsey20Kassoum Kayentao21Safiatou Doumbo22Aissata Ongoiba23Peter D Crompton24Boubacar Traore25Bryan Greenhouse26Silvia Portugal27Center for Infectious Diseases, Parasitology, Heidelberg University HospitalMax Planck Institute for Infection BiologyCenter for Infectious Diseases, Parasitology, Heidelberg University HospitalDepartment of Medicine, San Francisco General Hospital, University of CaliforniaCenter for Infectious Diseases, Parasitology, Heidelberg University HospitalCenter for Infectious Diseases, Parasitology, Heidelberg University HospitalMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoMax Planck Institute for Infection BiologyDepartment of Immunology and Infectious Diseases, Harvard TH Chan School of Public HealthLaboratory of Immunogenetics, NIAID, National Institutes of HealthMax Planck Institute for Infection BiologyMax Planck Institute for Infection BiologyMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoLaboratory of Immunogenetics, NIAID, National Institutes of HealthMax Planck Institute for Infection BiologyDivision of Infectious Diseases, Department of Medicine Solna, Karolinska Institute, Stockholm Sweden and Department of Infectious Diseases, Karolinska University HospitalMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoDivision of Infectious Diseases, Department of Medicine Solna, Karolinska Institute, Stockholm Sweden and Department of Infectious Diseases, Karolinska University HospitalZMBH, Heidelberg UniversityDepartment of Immunology and Infectious Diseases, Harvard TH Chan School of Public HealthMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoLaboratory of Immunogenetics, NIAID, National Institutes of HealthMali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of BamakoDepartment of Medicine, San Francisco General Hospital, University of CaliforniaCenter for Infectious Diseases, Parasitology, Heidelberg University HospitalAbstract 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.https://doi.org/10.1038/s44321-024-00127-wMalariaDry SeasonSensingInfection LengthAsymptomatic |
| spellingShingle | Carolina M Andrade Manuela Carrasquilla Usama Dabbas Jessica Briggs Hannah van Dijk Nikolay Sergeev Awa Sissoko Moussa Niangaly Christina Ntalla Emily LaVerriere Jeff Skinner Klara Golob Jeremy Richter Hamidou Cisse Shanping Li Jason A Hendry Muhammad Asghar Didier Doumtabe Anna Farnert Thomas Ruppert Daniel E Neafsey Kassoum Kayentao Safiatou Doumbo Aissata Ongoiba Peter D Crompton Boubacar Traore Bryan Greenhouse Silvia Portugal Infection length and host environment influence on Plasmodium falciparum dry season reservoir EMBO Molecular Medicine Malaria Dry Season Sensing Infection Length Asymptomatic |
| title | Infection length and host environment influence on Plasmodium falciparum dry season reservoir |
| title_full | Infection length and host environment influence on Plasmodium falciparum dry season reservoir |
| title_fullStr | Infection length and host environment influence on Plasmodium falciparum dry season reservoir |
| title_full_unstemmed | Infection length and host environment influence on Plasmodium falciparum dry season reservoir |
| title_short | Infection length and host environment influence on Plasmodium falciparum dry season reservoir |
| title_sort | infection length and host environment influence on plasmodium falciparum dry season reservoir |
| topic | Malaria Dry Season Sensing Infection Length Asymptomatic |
| url | https://doi.org/10.1038/s44321-024-00127-w |
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