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Genetic dissociation of three antigenic genes in Plasmodium ovale curtisi and Plasmodium ovale wallikeri.

ABSTRACT: Plasmodium ovale curtisi and Plasmodium ovale wallikeri are two sympatric human malaria species prevalent in Africa, Asia and Oceania. The reported prevalence of both P. ovale spp. was relatively low compared to other malaria species, but more sensitive molecular detection techniques have shown that asymptomatic low-density infections are more common than previously thought. Whole genome sequencing of both P. ovale spp. revealed genetic dissociation between P. ovale curtisi and P. ovale wallikeri suggesting a species barrier. In this study we further evaluate such a barrier by assessing polymorphisms in the genes of three vaccine candidate surface protein: circumsporozoite protein/ thrombospondin-related anonymous-related protein (ctrp), circumsporozoite surface protein (csp) and merozoite surface protein 1 (msp1). The complete coding sequence of ctrp and csp, and a partial fragment of msp1 were isolated from 25 P. ovale isolates and compared to previously reported reference sequences. A low level of nucleotide diversity (Pi = 0.02-0.10) was observed in all three genes. Various sizes of tandem repeats were observed in all ctrp, csp and msp1 genes. Both tandem repeat unit and nucleotide polymorphism in all three genes exhibited clear dimorphism between P. ovale curtisi and P. ovale wallikeri, supporting evidence of non-recombination between these two species.

SUBMITTER: Saralamba N

PROVIDER: S-EPMC6553752 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Genetic dissociation of three antigenic genes in Plasmodium ovale curtisi and Plasmodium ovale wallikeri.

Saralamba Naowarat N Nosten Francois F Sutherland Colin J CJ Arez Ana Paula AP Snounou Georges G White Nicholas J NJ Day Nicholas P J NPJ Dondorp Arjen M AM Imwong Mallika M

PloS one 20190606 6

Plasmodium ovale curtisi and Plasmodium ovale wallikeri are two sympatric human malaria species prevalent in Africa, Asia and Oceania. The reported prevalence of both P. ovale spp. was relatively low compared to other malaria species, but more sensitive molecular detection techniques have shown that asymptomatic low-density infections are more common than previously thought. Whole genome sequencing of both P. ovale spp. revealed genetic dissociation between P. ovale curtisi and P. ovale walliker ...[more]

PMID: 31170213

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Project description:BackgroundIn Ethiopia Plasmodium falciparum and Plasmodium vivax are the dominant species accounting for roughly 60 and 40% of malaria cases, respectively. Recently a major shift from P. falciparum to P. vivax has been observed in various parts of the country but the epidemiology of the other human malaria species, Plasmodium ovale spp. and Plasmodium malariae remains poorly understood. The aim of this study was to assess P. ovale curtisi and wallikeri infection in north-west Ethiopia by using microscopy and nested PCR.MethodsA health institution-based survey using non-probability sampling techniques was conducted at Maksegnet, Enfranze and Kola Diba health centres and Metema hospital in North Gondar. Three-hundred patients with signs and symptoms consistent with malaria were included in this study and capillary blood was collected for microscopic examination and molecular analysis of Plasmodium species. Samples were collected on Whatman 903 filter papers, stored in small plastic bags with desiccant and transported to Vienna (Austria) for molecular analysis. Data from study participants were entered and analysed by SPSS 20 software.ResultsOut of 300 study participants (167 males and 133 females), 184 samples were classified positive for malaria (133 P. falciparum and 51 P. vivax) by microscopy. By species-specific PCR 233 Plasmodium spp (95% CI: 72.6-82) were detected and the majority 155 (66.5%, 95% CI: 60.2-72.3) were P. falciparum followed by P. vivax 69 (29.6%, 95% CI; 24.1-35.8) and 9 (3.9%, 95% CI: 2-7.2) samples were positive for P. ovale. Seven of P. ovale parasites were confirmed as P. ovale wallikeri and two were confirmed as P. ovale curtisi. None of the samples tested positive for P. malariae. During microscopic examination there were high (16.3%) false negative reports and all mixed infections and P. ovale cases were missed or misclassified.ConclusionThis study indicates that P. ovale malaria is under-reported in Ethiopia and provides the first known evidence of the sympatric distribution of indigenous P. ovale wallikeri and P. ovale curtisi in Ethiopia. Therefore, further studies assessing the prevalence of the rare species P. ovale and P. malariae are urgently needed to better understand the species distribution and to adapt malaria control strategies.

Project description:Malaria caused by Plasmodium ovale species is considered a neglected tropical disease with limited information about its characteristics. It also remains unclear whether the two distinct species P. ovale curtisi and P. ovale wallikeri exhibit differences in their prevalence, geographic distribution, clinical characteristics, or laboratory parameters. Therefore, this study was conducted to clarify these differences to support global malaria control and eradication programs. Studies reporting the occurrence of P. ovale curtisi and P. ovale wallikeri were explored in databases. Differences in proportion, clinical data, and laboratory parameters between the two species were estimated using a random-effects model and expressed as pooled odds ratios (ORs), mean difference (MD), or standardized MD depending on the types of extracted data. The difference in geographical distribution was visualized by mapping the origin of the two species. A total of 1453 P. ovale cases extracted from 35 studies were included in the meta-analysis. The p-value in the meta-analyses provided evidence favoring a real difference between P. ovale curtisi malaria cases (809/1453, 55.7%) and P. ovale wallikeri malaria cases (644/1453, 44.3%) (p: 0.01, OR 1.61, 95% CI 0.71-3.63, I2: 77%). Subgroup analyses established evidence favoring a real difference between P. ovale curtisi and P. ovale wallikeri malaria cases among the imported cases (p: 0.02, 1135 cases). The p value in the meta-analyses provided evidence favoring a real difference in the mean latency period between P. ovale curtisi (289 cases) and P. ovale wallikeri malaria (266 cases) (p: 0.03, MD: 27.59, 95% CI 1.99-53.2, I2: 94%), total leukocyte count (p < 0.0001, MD: 840, 95% CI 610-1070, I2: 0%, two studies) and platelet count (p < 0.0001, MD: 44,750, 95% CI 2900-60,500, I2: 32%, three studies). Four continents were found to have reports of P. ovale spp., among which Africa had the highest number of reports for both P. ovale spp. in its 37 countries, with a global proportion of 94.46%, and an almost equal distribution of both P. ovale spp., where P. ovale curtisi and P. ovale wallikeri reflected 53.09% and 46.90% of the continent's proportion, respectively. This is the first systematic review and meta-analysis to demonstrate the differences in the characteristics of the two distinct P. ovale species. Malaria caused by P. ovale curtisi was found in higher proportions among imported cases and had longer latency periods, higher platelet counts, and higher total leukocyte counts than malaria caused by P. ovale wallikeri. Further studies with a larger sample size are required to confirm the differences or similarities between these two species to promote malaria control and effective eradication programs.

Project description:BackgroundPlasmodium ovale is relatively unfamiliar to Chinese staff engaged in malaria diagnosis. In 2013, dried blood spots of four unidentified but suspected ovale malaria samples were sent to the National Malaria Reference Laboratory (NMRL) for reconfirmation.MethodsPartial and complete, small, subunit ribosomal DNA (SSU rDNA) sequences of four samples were obtained with PCR-cloning-sequencing method. Obtained sequences were analyzed by aligning with each other and with nine SSU rDNA sequences of six known Plasmodium parasites. A phylogenetic tree was constructed based on complete SSU rDNA sequences and 12 same gene sequences derived from six known Plasmodium parasites and three Babesia parasites. Primary structure of conservative and variable regions of variant sequences was determined also by comparing them with those of six known Plasmodium parasites. To confirm their existence in genome, they were redetected with primers matching their variable regions. PCR systems aimed to roughly detect any eukaryotes and prokaryotes respectively were also applied to search for other pathogens in one of four patients.ResultsTotally, 19 partial and 23 complete SSU rDNA sequences obtained from four samples. Except eight variant sequences, similarities among sequences from same DNA sample were in general high (more than 98%). The phylogenetic analysis revealed that three cases were infected by P. ovale wallikeri and one by P. ovale curtisi. Four of the variant sequences which obtained from four samples relatively showed high similarities with each other (98.5%-100%). Identical variant sequences actually could be re-obtained from each DNA sample. Their primary structure of conservative and variable regions showed quite fit with that of six known Plasmodium parasites. The test for prokaryote pathogens showed negative and the tests for eukaryotes only found DNA sequences of Human and P. ovale parasites.ConclusionBoth P. ovale wallikeri and P. ovale curtisi infections are present in imported malaria cases of China. New type of partial SSU rDNA sequence which assumed to express in a certain life stage of P. ovale was obtained from both P. ovale wallikeri and P. ovale curtisi samples. This discovery would supply information and clues to identify and understand P. ovale parasites more accurately.

Dataset Information

Genetic dissociation of three antigenic genes in Plasmodium ovale curtisi and Plasmodium ovale wallikeri.

Publications

Genetic dissociation of three antigenic genes in Plasmodium ovale curtisi and Plasmodium ovale wallikeri.

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