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Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season.
Nat Med. 2020 Oct 26 [Online ahead of print]NMed

Abstract

The dry season is a major challenge for Plasmodium falciparum parasites in many malaria endemic regions, where water availability limits mosquito vectors to only part of the year. How P. falciparum bridges two transmission seasons months apart, without being cleared by the human host or compromising host survival, is poorly understood. Here we show that low levels of P. falciparum parasites persist in the blood of asymptomatic Malian individuals during the 5- to 6-month dry season, rarely causing symptoms and minimally affecting the host immune response. Parasites isolated during the dry season are transcriptionally distinct from those of individuals with febrile malaria in the transmission season, coinciding with longer circulation within each replicative cycle of parasitized erythrocytes without adhering to the vascular endothelium. Low parasite levels during the dry season are not due to impaired replication but rather to increased splenic clearance of longer-circulating infected erythrocytes, which likely maintain parasitemias below clinical and immunological radar. We propose that P. falciparum virulence in areas of seasonal malaria transmission is regulated so that the parasite decreases its endothelial binding capacity, allowing increased splenic clearance and enabling several months of subclinical parasite persistence.

Authors+Show Affiliations

Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany.Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, USA.Division of Infectious Diseases, Indiana University School of Medicine, Indianapolis, IN, USA.Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, USA.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, USA.Rocky Mountain Laboratory Research Technologies Section, Genomics Unit, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT, USA.Rocky Mountain Laboratory Research Technologies Section, Genomics Unit, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT, USA.Rocky Mountain Laboratory Research Technologies Section, Genomics Unit, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT, USA.Department of Medicine Solna, Division of Infectious Diseases, Karolinska Institutet, Stockholm, Sweden. Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.Department of Medicine Solna, Division of Infectious Diseases, Karolinska Institutet, Stockholm, Sweden. Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.Department of Immunology and Microbiology, Centre for Medical Parasitology, Faculty of Health and Medical Sciences, University of Copenhagen, København N, Denmark. Department of Infectious Diseases, Copenhagen University Hospital (Rigshospitalet), Copenhagen, Denmark.Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Portugal and ICVS/3B's -PT Government Associate Laboratory, Braga, Portugal.Department of Biochemistry and Molecular Biology, Huck Center for Malaria Research, The Pennsylvania State University, State College, PA, USA.Université de Paris, Institut Cochin, Paris, France.Institute of Global Health, Heidelberg University Hospital, Heidelberg, Germany.Department of Biochemistry and Molecular Biology, Huck Center for Malaria Research, The Pennsylvania State University, State College, PA, USA. Department of Chemistry, The Pennsylvania State University, State College, PA, USA.Université de Paris, Institut Cochin, Paris, France.Rocky Mountain Laboratory Research Technologies Section, Genomics Unit, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, MT, USA.Department of Medicine Solna, Division of Infectious Diseases, Karolinska Institutet, Stockholm, Sweden. Department of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Department of Immunology and Microbiology, Centre for Medical Parasitology, Faculty of Health and Medical Sciences, University of Copenhagen, København N, Denmark. Department of Infectious Diseases, Copenhagen University Hospital (Rigshospitalet), Copenhagen, Denmark.Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Portugal and ICVS/3B's -PT Government Associate Laboratory, Braga, Portugal.Institute of Infection, Immunity & Inflammation, MVLS, University of Glasgow, Glasgow, UK.Centre for Mathematics & the Environment, University of Exeter, Penryn Campus, Penryn, UK.Mali International Center of Excellence in Research, University of Sciences, Techniques and Technologies of Bamako, Bamako, Mali.Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD, USA.Center for Infectious Diseases, Parasitology, Heidelberg University Hospital, Heidelberg, Germany. portugal@mpiib-berlin.mpg.de. German Center for Infection Research (DZIF), Heidelberg, Heidelberg, Germany. portugal@mpiib-berlin.mpg.de. Max Planck Institute for Infection Biology, Berlin, Germany. portugal@mpiib-berlin.mpg.de.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

33106664

Citation

Andrade, Carolina M., et al. "Increased Circulation Time of Plasmodium Falciparum Underlies Persistent Asymptomatic Infection in the Dry Season." Nature Medicine, 2020.
Andrade CM, Fleckenstein H, Thomson-Luque R, et al. Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. Nat Med. 2020.
Andrade, C. M., Fleckenstein, H., Thomson-Luque, R., Doumbo, S., Lima, N. F., Anderson, C., Hibbert, J., Hopp, C. S., Tran, T. M., Li, S., Niangaly, M., Cisse, H., Doumtabe, D., Skinner, J., Sturdevant, D., Ricklefs, S., Virtaneva, K., Asghar, M., Homann, M. V., ... Portugal, S. (2020). Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. Nature Medicine. https://doi.org/10.1038/s41591-020-1084-0
Andrade CM, et al. Increased Circulation Time of Plasmodium Falciparum Underlies Persistent Asymptomatic Infection in the Dry Season. Nat Med. 2020 Oct 26; PubMed PMID: 33106664.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. AU - Andrade,Carolina M, AU - Fleckenstein,Hannah, AU - Thomson-Luque,Richard, AU - Doumbo,Safiatou, AU - Lima,Nathalia F, AU - Anderson,Carrie, AU - Hibbert,Julia, AU - Hopp,Christine S, AU - Tran,Tuan M, AU - Li,Shanping, AU - Niangaly,Moussa, AU - Cisse,Hamidou, AU - Doumtabe,Didier, AU - Skinner,Jeff, AU - Sturdevant,Dan, AU - Ricklefs,Stacy, AU - Virtaneva,Kimmo, AU - Asghar,Muhammad, AU - Homann,Manijeh Vafa, AU - Turner,Louise, AU - Martins,Joana, AU - Allman,Erik L, AU - N'Dri,Marie-Esther, AU - Winkler,Volker, AU - Llinás,Manuel, AU - Lavazec,Catherine, AU - Martens,Craig, AU - Färnert,Anna, AU - Kayentao,Kassoum, AU - Ongoiba,Aissata, AU - Lavstsen,Thomas, AU - Osório,Nuno S, AU - Otto,Thomas D, AU - Recker,Mario, AU - Traore,Boubacar, AU - Crompton,Peter D, AU - Portugal,Silvia, Y1 - 2020/10/26/ PY - 2020/04/02/received PY - 2020/08/27/accepted PY - 2020/10/28/pubmed PY - 2020/10/28/medline PY - 2020/10/27/entrez JF - Nature medicine JO - Nat Med N2 - The dry season is a major challenge for Plasmodium falciparum parasites in many malaria endemic regions, where water availability limits mosquito vectors to only part of the year. How P. falciparum bridges two transmission seasons months apart, without being cleared by the human host or compromising host survival, is poorly understood. Here we show that low levels of P. falciparum parasites persist in the blood of asymptomatic Malian individuals during the 5- to 6-month dry season, rarely causing symptoms and minimally affecting the host immune response. Parasites isolated during the dry season are transcriptionally distinct from those of individuals with febrile malaria in the transmission season, coinciding with longer circulation within each replicative cycle of parasitized erythrocytes without adhering to the vascular endothelium. Low parasite levels during the dry season are not due to impaired replication but rather to increased splenic clearance of longer-circulating infected erythrocytes, which likely maintain parasitemias below clinical and immunological radar. We propose that P. falciparum virulence in areas of seasonal malaria transmission is regulated so that the parasite decreases its endothelial binding capacity, allowing increased splenic clearance and enabling several months of subclinical parasite persistence. SN - 1546-170X UR - https://www.unboundmedicine.com/medline/citation/33106664/Increased_circulation_time_of_Plasmodium_falciparum_underlies_persistent_asymptomatic_infection_in_the_dry_season L2 - https://doi.org/10.1038/s41591-020-1084-0 DB - PRIME DP - Unbound Medicine ER -
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