Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: 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.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
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
_version_ 1784651151979839488
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
work_keys_str_mv AT tarimobrianb seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT nyasembevincento seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT ngasalabilly seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT bashamchristopher seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT rutagiisaackj seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT mullermeredith seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT chhetrisrijanab seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT rubinsteinrebecca seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT julianojonathanj seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT loyamwajabu seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT dinglasanrhoelr seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT linjessicat seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania
AT mathiasderrickk seasonalityandtransmissibilityofplasmodiumovaleinbagamoyodistricttanzania