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Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania
BACKGROUND: Plasmodium ovale is a neglected malarial parasite that can form latent hypnozoites in the human liver. Over the last decade, molecular surveillance studies of non-falciparum malaria in Africa have highlighted that P. ovale is circulating below the radar, including areas where Plasmodium...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8842944/ https://www.ncbi.nlm.nih.gov/pubmed/35164867 http://dx.doi.org/10.1186/s13071-022-05181-2 |
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author | Tarimo, Brian B. Nyasembe, Vincent O. Ngasala, Billy Basham, Christopher Rutagi, Isaack J. Muller, Meredith Chhetri, Srijana B. Rubinstein, Rebecca Juliano, Jonathan J. Loya, Mwajabu Dinglasan, Rhoel R. Lin, Jessica T. Mathias, Derrick K. |
author_facet | Tarimo, Brian B. Nyasembe, Vincent O. Ngasala, Billy Basham, Christopher Rutagi, Isaack J. Muller, Meredith Chhetri, Srijana B. Rubinstein, Rebecca Juliano, Jonathan J. Loya, Mwajabu Dinglasan, Rhoel R. Lin, Jessica T. Mathias, Derrick K. |
author_sort | Tarimo, Brian B. |
collection | PubMed |
description | BACKGROUND: Plasmodium ovale is a neglected malarial parasite that can form latent hypnozoites in the human liver. Over the last decade, molecular surveillance studies of non-falciparum malaria in Africa have highlighted that P. ovale is circulating below the radar, including areas where Plasmodium falciparum is in decline. To eliminate malaria where P. ovale is endemic, a better understanding of its epidemiology, asymptomatic carriage, and transmission biology is needed. METHODS: We performed a pilot study on P. ovale transmission as part of an ongoing study of human-to-mosquito transmission of P. falciparum from asymptomatic carriers. To characterize the malaria asymptomatic reservoir, cross-sectional qPCR surveys were conducted in Bagamoyo, Tanzania, over three transmission seasons. Positive individuals were enrolled in transmission studies of P. falciparum using direct skin feeding assays (DFAs) with Anopheles gambiae s.s. (IFAKARA strain) mosquitoes. For a subset of participants who screened positive for P. ovale on the day of DFA, we incubated blood-fed mosquitoes for 14 days to assess sporozoite development. RESULTS: Molecular surveillance of asymptomatic individuals revealed a P. ovale prevalence of 11% (300/2718), compared to 29% (780/2718) for P. falciparum. Prevalence for P. ovale was highest at the beginning of the long rainy season (15.5%, 128/826) in contrast to P. falciparum, which peaked later in both the long and short rainy seasons. Considering that these early-season P. ovale infections were low-density mono-infections (127/128), we speculate many were due to hypnozoite-induced relapse. Six of eight P. ovale-infected asymptomatic individuals who underwent DFAs successfully transmitted P. ovale parasites to A. gambiae. CONCLUSIONS: Plasmodium ovale is circulating at 4–15% prevalence among asymptomatic individuals in coastal Tanzania, largely invisible to field diagnostics. A different seasonal peak from co-endemic P. falciparum, the capacity to relapse, and efficient transmission to Anopheles vectors likely contribute to its persistence amid control efforts focused on P. falciparum. GRAPHICAL ABSTRACT: [Image: see text] |
format | Online Article Text |
id | pubmed-8842944 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-88429442022-02-16 Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania Tarimo, Brian B. Nyasembe, Vincent O. Ngasala, Billy Basham, Christopher Rutagi, Isaack J. Muller, Meredith Chhetri, Srijana B. Rubinstein, Rebecca Juliano, Jonathan J. Loya, Mwajabu Dinglasan, Rhoel R. Lin, Jessica T. Mathias, Derrick K. Parasit Vectors Short Report BACKGROUND: Plasmodium ovale is a neglected malarial parasite that can form latent hypnozoites in the human liver. Over the last decade, molecular surveillance studies of non-falciparum malaria in Africa have highlighted that P. ovale is circulating below the radar, including areas where Plasmodium falciparum is in decline. To eliminate malaria where P. ovale is endemic, a better understanding of its epidemiology, asymptomatic carriage, and transmission biology is needed. METHODS: We performed a pilot study on P. ovale transmission as part of an ongoing study of human-to-mosquito transmission of P. falciparum from asymptomatic carriers. To characterize the malaria asymptomatic reservoir, cross-sectional qPCR surveys were conducted in Bagamoyo, Tanzania, over three transmission seasons. Positive individuals were enrolled in transmission studies of P. falciparum using direct skin feeding assays (DFAs) with Anopheles gambiae s.s. (IFAKARA strain) mosquitoes. For a subset of participants who screened positive for P. ovale on the day of DFA, we incubated blood-fed mosquitoes for 14 days to assess sporozoite development. RESULTS: Molecular surveillance of asymptomatic individuals revealed a P. ovale prevalence of 11% (300/2718), compared to 29% (780/2718) for P. falciparum. Prevalence for P. ovale was highest at the beginning of the long rainy season (15.5%, 128/826) in contrast to P. falciparum, which peaked later in both the long and short rainy seasons. Considering that these early-season P. ovale infections were low-density mono-infections (127/128), we speculate many were due to hypnozoite-induced relapse. Six of eight P. ovale-infected asymptomatic individuals who underwent DFAs successfully transmitted P. ovale parasites to A. gambiae. CONCLUSIONS: Plasmodium ovale is circulating at 4–15% prevalence among asymptomatic individuals in coastal Tanzania, largely invisible to field diagnostics. A different seasonal peak from co-endemic P. falciparum, the capacity to relapse, and efficient transmission to Anopheles vectors likely contribute to its persistence amid control efforts focused on P. falciparum. GRAPHICAL ABSTRACT: [Image: see text] BioMed Central 2022-02-14 /pmc/articles/PMC8842944/ /pubmed/35164867 http://dx.doi.org/10.1186/s13071-022-05181-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Short Report Tarimo, Brian B. Nyasembe, Vincent O. Ngasala, Billy Basham, Christopher Rutagi, Isaack J. Muller, Meredith Chhetri, Srijana B. Rubinstein, Rebecca Juliano, Jonathan J. Loya, Mwajabu Dinglasan, Rhoel R. Lin, Jessica T. Mathias, Derrick K. Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title | Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title_full | Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title_fullStr | Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title_full_unstemmed | Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title_short | Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania |
title_sort | seasonality and transmissibility of plasmodium ovale in bagamoyo district, tanzania |
topic | Short Report |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8842944/ https://www.ncbi.nlm.nih.gov/pubmed/35164867 http://dx.doi.org/10.1186/s13071-022-05181-2 |
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