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

Yman, Victor; Wandell, Grace; Mutemi, Doreen D.; Miglar, Aurelie; Asghar, Muhammad; Hammar, Ulf; Karlsson, Mattias; Lind, Ingrid; Nordfjell, Cleis; Rooth, Ingegerd; Ngasala, Billy; Homann, Manijeh Vafa; Färnert, Anna

doi:10.1371/journal.pntd.0007414

Cited by 108 publications

(104 citation statements)

References 53 publications

(55 reference statements)

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“…As a result, the burden and population at risk in most endemic areas remain largely unknown. A recent study reported persistent detection of P. malariae over a 22-year period in an area of declining P. falciparum infections in Tanzania (9), suggesting that decline of P. falciparum could provide a favorable ecological niche for other malaria parasite species as also recently reported with the zoonotic malaria parasite species P. knowlesi in Malaysia (10).…”

Section: Introductionmentioning

confidence: 55%

Seroprevalence and parasite rates ofPlasmodium malariaein a high malaria transmission setting of southern Nigeria

Oriero

Olukosi

Oduwole

et al. 2019

Preprint

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BackgroundPlasmodium malariae is one of five malaria parasite species prevalent across sub-Saharan Africa, but with limited data on its prevalence and epidemiology across most endemic settings. Specific clinical diagnosis of P. malariae and other non-falciparum malaria parasites is uncommon and the most widely used malaria diagnostic tool, rapid diagnostic tests (RDTs), predominantly targets P. falciparum while nonspecifically identifying co-infecting species as 'pan-species'. Moreover, undetectable submicroscopic infections of these non-falciparum infections are likely and constitute a reservoir that could sustain transmission and challenge the achievement of elimination goals.This study aimed to explore prevalence of P. malariae infections in a high malaria transmission setting in Nigeria. MethodsA preliminary survey was first carried out in two sites to compare prevalence of non-falciparum species in southern Nigeria, results of which informed subsequent sample collection. Study participants were recruited from health facilities in Lagos and Calabar between October to December 2017 and subsequently from health facilities in four communities in Akpabuyo local government area of Cross River State, Nigeria from October -November 2018, following community sensitization and consent. Pan species RDT (SD Bioline, Cat No 05FK60) was used for field diagnosis and Thick blood films were also collected for microscopic detection of malaria parasites. Dried blood spots (DBS) collected from all participants were used for molecular detection of Plasmodium species by real-time PCR techniques. ResultsPlasmodium falciparum was most prevalent in the study populations, 22 -48% of all samples tested. From the primary survey, significantly higher prevalence of P. malariae and P. ovale were detected by qPCR in Calabar compared to Lagos. From a resampling of communities in Calabar, (N=798), Plasmodium spp infection prevalence by RDT was 23%. Non-falciparum infections detected was 12.5%, of which a median prevalence of 10.3% were infections with P. malariae (mixed and mono). The distribution of P. malariae infections between age groups (7.3 -16.1%) and communities (6.2 -12.1%) was heterogeneous. 32.9% of P. malariae infections occurred in the 11-15yrs age bracket, mostly as mixed infections. The odds of P. malariae as a mono infection was highest in the 0-5yrs age group relative to the group with the least odds of mono infections (11-15yrs). P. ovale was detected at 2.3%, while no sample tested positive for P. vivax. ConclusionsOverall, P. malariae was the most prevalent non-falciparum species and occurred mostly in the 11-15yrs age group, who are not targeted by some elimination strategies. Approaches for routine diagnosis of non-falciparum species in endemic settings will facilitate interventions towards panspecies malaria elimination.

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Section: Introductionmentioning

confidence: 55%

Seroprevalence and parasite rates ofPlasmodium malariaein a high malaria transmission setting of southern Nigeria

Oriero

Olukosi

Oduwole

et al. 2019

Preprint

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“…As the world moves towards reducing the malaria burden, the importance of mixed-species malaria infections will rise. Diagnostic techniques with improved sensitivities are revealing a greater prevalence of P. ovale and P. malariae in P. falciparum endemic areas than previously thought [7]. Intervention strategies such as anti-vector programs, and the development and employment of new drugs and vaccine will often be more effective against one species of parasite than they will against others [47,48].…”

Section: P Chabaudimentioning

confidence: 99%

“…The latter three species are parasites of non-human primates, but also cause zoonotic malaria in humans [1][2][3]. In large parts of the tropical world the ranges of at least some of these species overlap, they are often vectored by the same mosquitoes [4], and mixed-species infections are common [5][6][7].Mixed species infections of human malaria parasites are well-documented in natural [8][9][10][11][12] and experimental (e.g. [13,14]) settings.…”

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confidence: 99%

The consequences of mixed-species malaria parasite co-infections in mice and mosquitoes for disease severity, parasite fitness, and transmission success

Tang

Templeton

Cao

et al. 2019

Preprint

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The distributions of human malaria parasite species overlap in most malarious regions of the world, and co-infections involving two or more malaria parasite species are common. Little is known about the consequences of interactions between species during co-infection for disease severity and parasite transmission success. Anti-malarial interventions can have disproportionate effects on malaria parasite species, and may locally differentially reduce the number of species in circulation. Thus, it is important to have a clearer understanding of how the interactions between species affect disease and transmission dynamics. Controlled competition experiments using human malaria parasites are impossible, and thus we assessed the consequences of mixed-species infections on parasite fitness, disease severity, and transmission success using the rodent malaria parasite species Plasmodium chabaudi, P.yoelii yoelii, and P. vinckei lentum. We compared the fitness of individual species within single species and co-infections in mice. We also assessed the disease severity of single versus mixed infections in mice by measuring mortality rates, anaemia, and weight loss. Finally, we compared the transmission success of parasites in single or mixed species infections by quantifying oocyst development in Anopheles stephensi mosquitoes. We found that coinfections of P. yoelii with either P. vinckei or P. chabaudi led to a dramatic increase in infection virulence, with 100% mortality observed in mixed species infections, compared to no mortality for P. yoelii and P. vinckei single infections, and 40% mortality for P. chabaudi single infections. The increased mortality in the mixed infections was associated with an inability to clear parasitaemia, with the non-P. yoelii parasite species persisting at higher parasite densities than in single infections. P. yoelii growth was suppressed in all mixed infections compared to single infections. Transmissibility of P. vinckei and P. chabaudi to mosquitoes was also reduced in the presence of P. yoelii in co-infections compared to single infections. The increased virulence of co-infections containing P. yoelii (reticulocyte restricted) and P. chabaudi or P. vinckei (predominantly normocyte restricted) may be due to parasite cell tropism and/or immune modulation of the host. We explain the reduction in transmission success of species in co-infections in terms of inter-species gamete incompatibility.Eight malaria parasite species are infectious to humans; namely, Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale wallikeri, Plasmodium ovale curtisii, Plasmodium knowlesi, Plasmodium cynomolgi, and Plasmodium simium. The latter three species are parasites of non-human primates, but also cause zoonotic malaria in humans [1][2][3]. In large parts of the tropical world the ranges of at least some of these species overlap, they are often vectored by the same mosquitoes [4], and mixed-species infections are common [5][6][7].Mixed species infections of human malaria parasites a...

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“…Western Pacific [2][3][4]. It has been argued that malaria elimination programmes largely focused on Plasmodium falciparum and Plasmodium vivax may have undermined P. malariae and Plasmodium ovale endemicity [5]. Plasmodium malariae deploys a different transmission strategy, with a large parasite reservoir in asymptomatic carriers with low parasitaemia.…”

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confidence: 99%

Polymorphic markers for identification of parasite population in Plasmodium malariae

Mathema

Nakeesathit

Pagornrat

et al. 2020

Malar J

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Background: Molecular genotyping in Plasmodium serves many aims including providing tools for studying parasite population genetics and distinguishing recrudescence from reinfection. Microsatellite typing, insertion-deletion (INDEL) and single nucleotide polymorphisms is used for genotyping, but only limited information is available for Plasmodium malariae, an important human malaria species. This study aimed to provide a set of genetic markers to facilitate the study of P. malariae population genetics. Methods: Markers for microsatellite genotyping and pmmsp1 gene polymorphisms were developed and validated in symptomatic P. malariae field isolates from Myanmar (N = 37). Fragment analysis was used to determine allele sizes at each locus to calculate multiplicity of infections (MOI), linkage disequilibrium, heterozygosity and construct dendrograms. Nucleotide diversity (π), number of haplotypes, and genetic diversity (H d) were assessed and a phylogenetic tree was constructed. Genome-wide microsatellite maps with annotated regions of newly identified markers were constructed. Results: Six microsatellite markers were developed and tested in 37 P. malariae isolates which showed sufficient heterozygosity (0.530-0.922), and absence of linkage disequilibrium (I A S =0.03, p value > 0.05) (N = 37). In addition, a tandem repeat (VNTR)-based pmmsp1 INDEL polymorphisms marker was developed and assessed in 27 P. malariae isolates showing a nucleotide diversity of 0.0976, haplotype gene diversity of 0.698 and identified 14 unique variants. The size of VNTR consensus repeat unit adopted as allele was 27 base pairs. The markers Pm12_426 and pmmsp1 showed greatest diversity with heterozygosity scores of 0.920 and 0.835, respectively. Using six microsatellites markers, the likelihood that any two parasite strains would have the same microsatellite genotypes was 8.46 × 10 −4 and was further reduced to 1.66 × 10 −4 when pmmsp1 polymorphisms were included. Conclusions: Six novel microsatellites genotyping markers and a set of pmmsp1 VNTR-based INDEL polymorphisms markers for P. malariae were developed and validated. Each marker could be independently or in combination employed to access genotyping of the parasite. The newly developed markers may serve as a useful tool for investigating parasite diversity, population genetics, molecular epidemiology and for distinguishing recrudescence from reinfection in drug efficacy studies.

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

Cited by 108 publications

References 53 publications

Seroprevalence and parasite rates ofPlasmodium malariaein a high malaria transmission setting of southern Nigeria

Seroprevalence and parasite rates ofPlasmodium malariaein a high malaria transmission setting of southern Nigeria

The consequences of mixed-species malaria parasite co-infections in mice and mosquitoes for disease severity, parasite fitness, and transmission success

Polymorphic markers for identification of parasite population in Plasmodium malariae

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