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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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

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

Related collections

Malaria vaccine development

Most cited references 17

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

Plasmodium ovale: parasite and disease.

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

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