Seasonality and transmissibility of <i>Plasmodium ovale</i> in Bagamoyo District, Tanzania

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Abstract

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.

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Most cited references 15

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Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally.

Colin J Sutherland, Naowarat Tanomsing, Spencer N. White … (2010)

Malaria in humans is caused by apicomplexan parasites belonging to 5 species of the genus Plasmodium. Infections with Plasmodium ovale are widely distributed but rarely investigated, and the resulting burden of disease is not known. Dimorphism in defined genes has led to P. ovale parasites being divided into classic and variant types. We hypothesized that these dimorphs represent distinct parasite species. Multilocus sequence analysis of 6 genetic characters was carried out among 55 isolates from 12 African and 3 Asia-Pacific countries. Each genetic character displayed complete dimorphism and segregated perfectly between the 2 types. Both types were identified in samples from Ghana, Nigeria, São Tomé, Sierra Leone, and Uganda and have been described previously in Myanmar. Splitting of the 2 lineages is estimated to have occurred between 1.0 and 3.5 million years ago in hominid hosts. We propose that P. ovale comprises 2 nonrecombining species that are sympatric in Africa and Asia. We speculate on possible scenarios that could have led to this speciation. Furthermore, the relatively high frequency of imported cases of symptomatic P. ovale infection in the United Kingdom suggests that the morbidity caused by ovale malaria has been underestimated.

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Plasmodium malariae and P. ovale genomes provide insights into malaria parasite evolution

Gavin Rutledge, Ulrike Böhme, Mandy Sanders … (2017)

Elucidation of the evolutionary history and interrelatedness of Plasmodium species that infect humans has been hampered by a lack of genetic information for three human-infective species: P. malariae and two P. ovale species (P. o. curtisi and P. o. wallikeri)1. These species are prevalent across most regions in which malaria is endemic2,3 and are often undetectable by light microscopy4, rendering their study in human populations difficult5. The exact evolutionary relationship of these species to the other human-infective species has been contested6,7. Using a new reference genome for P. malariae and a manually curated draft P. o. curtisi genome, we are now able to accurately place these species within the Plasmodium phylogeny. Sequencing of a P. malariae relative that infects chimpanzees reveals similar signatures of selection in the P. malariae lineage to another Plasmodium lineage shown to be capable of colonization of both human and chimpanzee hosts. Molecular dating suggests that these host adaptations occurred over similar evolutionary timescales. In addition to the core genome that is conserved between species, differences in gene content can be linked to their specific biology. The genome suggests that P. malariae expresses a family of heterodimeric proteins on its surface that have structural similarities to a protein crucial for invasion of red blood cells. The data presented here provide insight into the evolution of the Plasmodium genus as a whole.

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Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania

Victor Yman, Grace Wandell, Doreen D. Mutemi … (2019)

A reduction in the global burden of malaria over the past two decades has encouraged efforts for regional malaria elimination. Despite the need to target all Plasmodium species, current focus is mainly directed towards Plasmodium falciparum, and to a lesser extent P. vivax. There is a substantial lack of data on both global and local transmission patterns of the neglected malaria parasites P. malariae and P. ovale spp. We used a species-specific real-time PCR assay targeting the Plasmodium 18s rRNA gene to evaluate temporal trends in the prevalence of all human malaria parasites over a 22-year period in a rural village in Tanzania.We tested 2897 blood samples collected in five cross-sectional surveys conducted between 1994 and 2016. Infections with P. falciparum, P. malariae, and P. ovale spp. were detected throughout the study period, while P. vivax was not detected. Between 1994 and 2010, we found a more than 90% reduction in the odds of infection with all detected species. The odds of P. falciparum infection was further reduced in 2016, while the odds of P. malariae and P. ovale spp. infection increased 2- and 6-fold, respectively, compared to 2010. In 2016, non-falciparum species occurred more often as mono-infections. The results demonstrate the persistent transmission of P. ovale spp., and to a lesser extent P. malariae despite a continued decline in P. falciparum transmission. This illustrates that the transmission patterns of the non-falciparum species do not necessarily follow those of P. falciparum, stressing the need for attention towards non-falciparum malaria in Africa. Malaria elimination will require a better understanding of the epidemiology of P. malariae and P. ovale spp. and improved tools for monitoring the transmission of all Plasmodium species, with a particular focus towards identifying asymptomatic carriers of infection and designing appropriate interventions to enhance malaria control.

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Author and article information

Contributors

Brian B. Tarimo: btarimo@ihi.or.tz

Vincent O. Nyasembe: vnyasembe@ufl.edu

Billy Ngasala: bngasala70@yahoo.co.uk

Christopher Basham: christopher_basham@med.unc.edu

Isaack J. Rutagi: isaacjohn830@gmail.com

Meredith Muller: meredith_muller@med.unc.edu

Srijana B. Chhetri: srijana.bhattaraichhetri2@unchealth.unc.edu

Rebecca Rubinstein: rebecca_rubinstein@med.unc.edu

Jonathan J. Juliano: jonathan_juliano@med.unc.edu

Mwajabu Loya: loyamwajabu51@gmail.com

Rhoel R. Dinglasan: rdinglasan@epi.ufl.edu

Jessica T. Lin: linjt@email.unc.edu

Derrick K. Mathias:

ORCID: http://orcid.org/0000-0002-8743-7285

d.mathias@ufl.edu

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 14 February 2022

Publication date PMC-release: 14 February 2022

Publication date Collection: 2022

Volume: 15

Electronic Location Identifier: 56

Affiliations

[1 ]GRID grid.414543.3, ISNI 0000 0000 9144 642X, Vector Immunity and Transmission Biology Unit, Department of Environmental Health and Ecological Science, , Ifakara Health Institute-Bagamoyo Office, ; P.O. Box 74, Bagamoyo, Coast Region 61301 Tanzania

[2 ]GRID grid.15276.37, ISNI 0000 0004 1936 8091, Department of Infectious Diseases and Immunology, College of Veterinary Medicine, , Emerging Pathogens Institute, University of Florida, ; Gainesville, FL 32611 USA

[3 ]GRID grid.25867.3e, ISNI 0000 0001 1481 7466, Department of Parasitology and Medical Entomology, School of Public Health and Social Sciences, , Muhimbili University of Health and Allied Sciences, ; Dar es Salaam, 11103 Tanzania

[4 ]GRID grid.10698.36, ISNI 0000000122483208, Institute of Global Health and Infectious Diseases, , University of North Carolina School of Medicine, ; Chapel Hill, NC 27599 USA

[5 ]GRID grid.15276.37, ISNI 0000 0004 1936 8091, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Institute of Food and Agricultural Sciences, , University of Florida, ; Vero Beach, FL 32962 USA

Author information

Derrick K. Mathias http://orcid.org/0000-0002-8743-7285

Article

Publisher ID: 5181

DOI: 10.1186/s13071-022-05181-2

PMC ID: 8842944

PubMed ID: 35164867

SO-VID: 84a859ef-2c80-436d-b724-0443f5f916aa

License:

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/. The Creative Commons Public Domain Dedication waiver ( http://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.

History

Date received : 9 September 2021

Date accepted : 12 December 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;

Award ID: R01AI137395

Award Recipient : Jessica T. Lin

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: plasmodium ovale,plasmodium falciparum,malaria,asymptomatic,tanzania,anopheles gambiae,direct feeding assay (dfa)

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: plasmodium ovale, plasmodium falciparum, malaria, asymptomatic, tanzania, anopheles gambiae, direct feeding assay (dfa)

Seasonality and transmissibility of Plasmodium ovale in Bagamoyo District, Tanzania

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Abstract

Background

Methods

Results

Conclusions

Graphical Abstract

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Malaria vaccine development

Most cited references 15

Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally.

Plasmodium malariae and P. ovale genomes provide insights into malaria parasite evolution

Persistent transmission of Plasmodium malariae and Plasmodium ovale species in an area of declining Plasmodium falciparum transmission in eastern Tanzania

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