Prevalence of non- <i>falciparum</i> malaria infections among asymptomatic individuals in four regions of Mainland Tanzania

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Abstract

Background

Recent studies point to the need to incorporate the detection of non-falciparum species into malaria surveillance activities in sub-Saharan Africa, where 95% of the world’s malaria cases occur. Although malaria caused by infection with Plasmodium falciparum is typically more severe than malaria caused by the non-falciparum Plasmodium species P. malariae, P. ovale spp. and P. vivax, the latter may be more challenging to diagnose, treat, control and ultimately eliminate. The prevalence of non-falciparum species throughout sub-Saharan Africa is poorly defined. Tanzania has geographical heterogeneity in transmission levels but an overall high malaria burden.

Methods

To estimate the prevalence of malaria species in Mainland Tanzania, we randomly selected 1428 samples from 6005 asymptomatic isolates collected in previous cross-sectional community surveys across four regions and analyzed these by quantitative PCR to detect and identify the Plasmodium species.

Results

Plasmodium falciparum was the most prevalent species in all samples, with P. malariae and P. ovale spp. detected at a lower prevalence (< 5%) in all four regions; P. vivax was not detected in any sample.

Conclusions

The results of this study indicate that malaria elimination efforts in Tanzania will need to account for and enhance surveillance of these non-falciparum species.

Graphical Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-024-06242-4.

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Most cited references 17

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School-Age Children Are a Reservoir of Malaria Infection in Malawi

Jenny A. Walldorf, Lauren Cohee, Jenna E. Coalson … (2015)

Malaria surveillance and interventions in endemic countries often target young children at highest risk of malaria morbidity and mortality. We aimed to determine whether school-age children and adults not captured in surveillance serve as a reservoir for malaria infection and may contribute to malaria transmission. Cross-sectional surveys were conducted in one rainy and one dry season in southern Malawi. Demographic and health information was collected for all household members. Blood samples were obtained for microscopic and PCR identification of Plasmodium falciparum. Among 5796 individuals aged greater than six months, PCR prevalence of malaria infection was 5%, 10%, and 20% in dry, and 9%, 15%, and 32% in rainy seasons in Blantyre, Thyolo, and Chikhwawa, respectively. Over 88% of those infected were asymptomatic. Participants aged 6–15 years were at higher risk of infection (OR=4.8; 95%CI, 4.0–5.8) and asymptomatic infection (OR=4.2; 95%CI, 2.7–6.6) than younger children in all settings. School-age children used bednets less frequently than other age groups. Compared to young children, school-age children were brought less often for treatment and more often to unreliable treatment sources. Conclusion: School-age children represent an underappreciated reservoir of malaria infection and have less exposure to antimalarial interventions. Malaria control and elimination strategies may need to expand to include this age group.

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Plasmodium ovale: parasite and disease.

G. Jeffery, James W. Collins (2005)

Humans are infected by four recognized species of malaria parasites. The last of these to be recognized and described is Plasmodium ovale. Like the other malaria parasites of primates, this parasite is only transmitted via the bites of infected Anopheles mosquitoes. The prepatent period in the human ranges from 12 to 20 days. Some forms in the liver have delayed development, and relapse may occur after periods of up to 4 years after infection. The developmental cycle in the blood lasts approximately 49 h. An examination of records from induced infections indicated that there were an average of 10.3 fever episodes of > or = 101 degrees F and 4.5 fever episodes of > or = 104 degrees F. Mean maximum parasite levels were 6,944/microl for sporozoite-induced infections and 7,310/microl for trophozoite-induced infections. Exoerythrocytic stages have been demonstrated in the liver of humans, chimpanzees, and Saimiri monkeys following injection of sporozoites. Many different Anopheles species have been shown to be susceptible to infection with P. ovale, including A. gambiae, A. atroparvus, A. dirus, A. freeborni, A. albimanus, A. quadrimaculatus, A. stephensi, A. maculatus, A. subpictus, and A. farauti. An enzyme-linked immunosorbent assay has been developed to detect mosquitoes infected with P. ovale using a monoclonal antibody directed against the circumsporozoite protein. Plasmodium ovale is primarily distributed throughout sub-Saharan Africa. It has also been reported from numerous islands in the western Pacific. In more recent years, there have been reports of its distribution on the Asian mainland. Whether or not it will become a major public health problem there remains to be seen. The diagnosis of P. ovale is based primarily on the characteristics of the blood stages and its differentiation from P. vivax. The sometimes elliptical shape of the infected erythrocyte is often diagnostic when combined with other, subtler differences in morphology. The advent of molecular techniques, primarily PCR, has made diagnostic confirmation possible. The development of techniques for the long-term frozen preservation of malaria parasites has allowed the development diagnostic reference standards for P. ovale. Infections in chimpanzees are used to provide reference and diagnostic material for serologic and molecular studies because this parasite has not been shown to develop in other nonhuman primates, nor has it adapted to in vitro culture. There is no evidence to suggest that P. ovale is closely related phylogenetically to any other of the primate malaria parasites that have been examined.

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Sources of persistent malaria transmission in a setting with effective malaria control in eastern Uganda: a longitudinal, observational cohort study

Chiara Andolina, John Rek, Jessica Briggs … (2021)

Background Symptomatic malaria cases reflect only a small proportion of all Plasmodium spp infections. Many infected individuals are asymptomatic, and persistent asymptomatic Plasmodium falciparum infections are common in endemic settings. We aimed to quantify the contribution of symptomatic and asymptomatic infections to P falciparum transmission in Tororo, Uganda. Methods We did a longitudinal, observational cohort study in Tororo district, Uganda. We recruited participants of all ages from randomly selected households within this district. Participants were eligible if the selected household had no more than nine permanent residents and at least two members younger than 10 years, and the household was their primary residence, and they agreed to come to the study clinic for any fever episode and avoid antimalarial medications outside the study. Participants were followed-up by continuous passive surveillance for the incidence of symptomatic infections; routine assessments (ie, standardised clinical evaluation and blood samples) were done at baseline and at routine visits every 4 weeks for 2 years. P falciparum parasite density, gametocyte density, and genetic composition were determined molecularly using quantitative PCR (qPCR), quantitative reverse transcriptase PCR (qRT-PCR), and amplicon deep sequencing, respectively. Membrane feeding assays were also done to assess infectivity to mosquitoes. The contribution of different populations to the infectious reservoir was estimated for symptomatic infections, asymptomatic but microscopically detected infections, and asymptomatic but qPCR-detected infections; and for age groups younger than 5 years, 5–15 years, and 16 years or older. Findings Between Oct 4, 2017, and Oct 31, 2019, 531 individuals were enrolled from 80 randomly selected households and were followed-up for 2 years. At baseline, P falciparum was detected in 28 (5·3%) of 531 participants by microscopy and an additional 64 (12·1%) by qPCR and declined thereafter. In 538 mosquito feeding experiments on 107 individuals, 446 (1·2%) of 37 404 mosquitoes became infected, with mosquito infection rates being strongly associated with gametocyte densities (β=2·11, 95% CI 1·62–2·67; p<0·0001). Considering both transmissibility of infections and their relative frequency, the estimated human infectious reservoir consisted primarily of asymptomatic microscopy-detected infections (83·8%), followed by asymptomatic submicroscopic infections (15·6%), and symptomatic infections (0·6%). Children aged 5–15 years accounted for more than half of the infectious reservoir (58·7%); individuals younger than 5 years (25·8%) and those 16 years or older (15·6%) contributed less. Samples from four children contribued to 279 (62·6%) of 446 infected mosquitoes after multiple mosquito-feeding assays. Interpretation Individuals with asymptomatic infections were important drivers of malaria transmission. School-aged children contributed to more than half of all mosquito infections, with a small minority of asymptomatic children being highly infectious. Demographically targeted interventions, aimed at school-aged children, could further reduce transmission in areas under effective vector control. Funding US National Institutes of Health, Bill & Melinda Gates Foundation, and the European Research Council.

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Author and article information

Contributors

Zachary R. Popkin-Hall: zach_popkin-hall@med.unc.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): 23 March 2024

Publication date PMC-release: 23 March 2024

Publication date Collection: 2024

Volume: 17

Electronic Location Identifier: 153

Affiliations

[1 ]Institute for Global Health and Infectious Diseases, University of North Carolina, ( https://ror.org/0130frc33) Chapel Hill, NC USA

[2 ]National Institute for Medical Research, ( https://ror.org/05fjs7w98) Dar es Salaam, Tanzania

[3 ]National Institute for Medical Research, Tanga Center, ( https://ror.org/05fjs7w98) Tanga, Tanzania

[4 ]The Connecticut Agricultural Experiment Station, ( https://ror.org/02t7c5797) New Haven, CT USA

[5 ]GRID grid.415734.0, ISNI 0000 0001 2185 2147, National Malaria Control Programme, ; Dodoma, Tanzania

[6 ]Department of Pathology and Laboratory Medicine, Warren Alpert Medical School, Brown University, ( https://ror.org/05gq02987) Providence, RI USA

[7 ]Center for Computational Molecular Biology, Brown University, ( https://ror.org/05gq02987) Providence, RI USA

[8 ]GRID grid.416738.f, ISNI 0000 0001 2163 0069, Malaria Branch, National Center for Emerging and Zoonotic Infectious Diseases, , US Centers for Disease Control and Prevention (CDC), ; Atlanta, GA USA

[9 ]GRID grid.38142.3c, ISNI 000000041936754X, Harvard T.H. Chan School of Public Health, ; Boston, MA USA

[10 ]Faculty of Pharmaceutical Sciences, Monash University, ( https://ror.org/02bfwt286) Melbourne, VIC Australia

Article

Publisher ID: 6242

DOI: 10.1186/s13071-024-06242-4

PMC ID: 10960463

PubMed ID: 38519992

SO-VID: 5624236c-213b-4c21-94fe-685cc8dc154a

License:

Open Access This 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 : 29 December 2023

Date accepted : 11 March 2024

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;

Award ID: 002202

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: K24AI134990

Award Recipient : Jonathan J. Juliano

Funded by: FundRef http://dx.doi.org/10.13039/100019778, President's Malaria Initiative;

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: malaria,plasmodium malariae,plasmodium ovale,plasmodium vivax,non-falciparum species,tanzania,asymptomatic malaria

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: malaria, plasmodium malariae, plasmodium ovale, plasmodium vivax, non-falciparum species, tanzania, asymptomatic malaria

Prevalence of non- falciparum malaria infections among asymptomatic individuals in four regions of Mainland Tanzania

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Abstract

Background

Methods

Results

Conclusions

Graphical Abstract

Supplementary Information

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Malaria vaccine development

Most cited references 17

School-Age Children Are a Reservoir of Malaria Infection in Malawi

Plasmodium ovale: parasite and disease.

Sources of persistent malaria transmission in a setting with effective malaria control in eastern Uganda: a longitudinal, observational cohort study

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