Outbreak of human malaria caused by Plasmodium simium in the Atlantic Forest in Rio de Janeiro: a molecular epidemiological investigation

Brasil, Patrícia; Zalis, Mariano Gustavo; Pina-Costa, Anielle de; Siqueira, André Machado; Júnior, Cesare Bianco; Silva, Sidnei G.; Areas, André Luiz Lisboa; Pelajo-Machado, Marcelo; Alvarenga, Denise Anete Madureira de; Santelli, Ana Carolina Faria da Silva; Albuquerque, Hermano Gomes; Cravo, Pedro Vitor Lemos; Abreu, Filipe Vieira Santos de; Peterka, Cassio; Zaniní, Graziela Maria; Suárez-Mútis, Martha Cecília; Pissinatti, Alcides; Lourenço‐de‐Oliveira, Ricardo; Brito, Cristiana Ferreira Alves de; Ferreira-da-Cruz, Maria de Fátima; Culleton, Richard; Daniel-Ribeiro, Cláudio Tadeu

doi:10.1016/s2214-109x(17)30333-9

Cited by 205 publications

(284 citation statements)

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“…During this period, P. knowlesi zoonosis has increased in Southeast Asia [38], and a growing body of evidence suggests that monkey-to-human transmission of P. simium has produced malaria outbreaks in areas of Brazil where elimination had been achieved [72]. While the public health community has traditionally ignored animal reservoirs in the context of malaria eradication, it is our position that the impetus to systematically evaluate the risk of malaria zoonosis has never been greater.…”

Section: Discussionmentioning

confidence: 99%

“…If confirmed, New World monkeys could represent an ongoing source of human P. vivax/P. simium infection [70,72], potentially forming a major hurdle to malaria control efforts in South America. However, functional assays will be necessary to confirm this hypothesis, and progress may be slow until a continuous in vitro P. vivax culture system is developed [73].…”

Section: Plasmodium Vivax: a Long Neglected Pandemicmentioning

confidence: 99%

“…Four malaria parasites (i.e., P. falciparum, P. vivax, P. malariae, P. ovale ) have adapted to the human population and are transmissible among human hosts [2]. Cross-species transmission of three primate species (i.e., P. knowlesi [3,4], P. simium [72], P. brasilianum [77]) have been documented with increasing frequency during recent years. While it appears that these species are either incapable of human-to-human transmission or produce stuttering transmission chains in the human population, subsequent adaption may facilitate emergence.…”

Section: Figurementioning

confidence: 99%

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Molecular interactions governing host-specificity of blood stage malaria parasites

Scully

Kanjee

Duraisingh

2017

Current Opinion in Microbiology

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Non-human primates harbor diverse species of malaria parasites, including the progenitors of P. falciparum and P. vivax. Cross-species transmission of some malaria parasites—most notably the macaque parasite, P. knowlesi—continues to this day, compelling the scientific community to ask whether these zoonoses could impede malaria control efforts by acting as a source of recurrent human infection. Host-restriction varies considerably among parasite species and is governed by both ecological and molecular variables. In particular, the efficiency of red blood cell invasion constitutes a prominent barrier to zoonotic emergence. Although proteins expressed upon the erythrocyte surface exhibit considerable diversity both within and among hosts, malaria parasites have adapted to this heterogeneity via the expansion of protein families associated with invasion, offering redundant mechanisms of host cell entry. This molecular toolkit may enable some parasites to circumvent host barriers, potentially yielding host shifts upon subsequent adaptation. Recent studies have begun to elucidate the molecular determinants of host-specificity, as well as the mechanisms that malaria parasites use to overcome these restrictions. We review recent studies concerning host tropism in the context of erythrocyte invasion by focusing on three malaria parasites that span the zoonotic spectrum: P. falciparum, P. knowlesi, and P. vivax.

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Section: Discussionmentioning

confidence: 99%

Section: Plasmodium Vivax: a Long Neglected Pandemicmentioning

confidence: 99%

Section: Figurementioning

confidence: 99%

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Molecular interactions governing host-specificity of blood stage malaria parasites

Scully

Kanjee

Duraisingh

2017

Current Opinion in Microbiology

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“…There are currently eight species of malaria parasites known to cause disease in humans; Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale curtisi, Plasmodium ovale wallikeri, Plasmodium knowlesi, Plasmodium cynomolgi and Plasmodium simium . The latter three species are more commonly parasitic on non-human primates and have only relatively recently been shown to infect humans 1-3 .…”

Section: Introductionmentioning

confidence: 99%

The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host-switching

Mourier

Alvarenga

Kaushik

et al. 2019

Preprint

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Oxford, Headington, Oxford, OX3 9DU, UK 41 42 §) Contributed equally, arranged alphabetically 43 †) Corresponding authors 44 45 46 Summary 47 48 Plasmodium simium, a malaria parasite of non-human primates in the Atlantic forest region of 49Brazil was recently shown to cause zoonotic infection in humans in the region. Phylogenetic 50 analyses based on the whole genome sequences of six P. simium isolates infecting humans 51 and two isolates from brown howler monkeys revealed that P. simium is monophyletic within 52 the broader diversity of South American Plasmodium vivax, consistent with the hypothesis 53 that P. simium first infected non-human primates as a result of a host-switch from humans 54 carrying P. vivax. We provide molecular evidence that the current zoonotic infections of 55 people have likely resulted from multiple independent host switches, each seeded from a 56 different monkey infection. Very low levels of genetic diversity within P. simium genomes 57 and the absence of P. simium-P. vivax hybrids suggest that the P. simium population emerged 58 recently and has subsequently experienced a period of independent evolution in Platyrrhini 59 monkeys. We further find that Plasmodium Interspersed Repeat (PIR) genes, Plasmodium 60Helical Interspersed Subtelomeric (PHIST) genes and Tryptophan-Rich Antigens (TRAg) 61 genes in P. siumium are genetically divergent from P. vivax and are enriched for non-62 synonymous single nucleotide polymorphisms, consistent with the rapid evolution of these 63 genes. Analysis of genes involved in erythrocyte invasion revealed several notable differences 64 between P. vivax and P. simium, including large deletions within the coding region of the 65 Duffy Binding Protein 1 (DBP1) and Reticulocyte Binding Protein 2a (RBP2a) genes in P. 66 simium. Genotyping of P. simium isolates from non-human primates (NHPs) and zoonotic 67 human infections showed that a precise deletion of 38 amino acids in DBP1 is exclusively 67 present in all human infecting isolates, whereas non-human primate infecting isolates were 68 polymorphic for the deletion. We speculate that these deletions in the parasite-encoded key 69 erythrocyte invasion ligands and the additional rapid genetic changes have facilitated zoonotic 70 transfer to humans. Non-human primate malaria parasites can be considered a reservoir of 71 potential infectious human parasites that must be considered in any attempt of malaria 72 elimination. The genome of P. simium will thus form an important basis for future functional 73 characterizations on the mechanisms underlying malaria zoonosis. 74 75 76 Introduction 77 78 There are currently eight species of malaria parasites known to cause disease in humans; 79 Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale 80 curtisi, Plasmodium ovale wallikeri, Plasmodium knowlesi, Plasmodium cynomolgi and 81 Plasmodium simium. The latter three species are more commonly parasitic on non-human 82 primates and have only relatively recently been shown to infect humans 1-3 . ...

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“…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 are well-documented in natural [8][9][10][11][12] and experimental (e.g.…”

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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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Outbreak of human malaria caused by Plasmodium simium in the Atlantic Forest in Rio de Janeiro: a molecular epidemiological investigation

Cited by 205 publications

References 23 publications

Molecular interactions governing host-specificity of blood stage malaria parasites

Molecular interactions governing host-specificity of blood stage malaria parasites

The genome of the zoonotic malaria parasite Plasmodium simium reveals adaptations to host-switching

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

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