Plasmodium simium/Plasmodium vivax infections in southern brown howler monkeys from the Atlantic Forest

Costa, Daniela Camargos; Cunha, Vanessa Pecini da; Assis, Gabriela Maria Pereira de; Souza, Júlio César de; Hirano, Zelinda Maria Braga; Arruda, Maria Augusta; Kano, Flora Satiko; Carvalho, Luzia H.; Brito, Cristiana Ferreira Alves de

doi:10.1590/0074-0276130578

Cited by 27 publications

(57 citation statements)

References 19 publications

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“…The frequency of P. simium infection in free-living howler monkeys in RJ (16.6%) was higher than that found in the bordering state of SP (5.8%) but lower than that found in the entire southern and southeastern Brazilian regions (26.3-35%) [5,20,37]. A. g. clamitans was also the only free-living NHP from RJ in which blood forms by microscopy and plasmodial DNA were detected.…”

Section: Discussionmentioning

confidence: 78%

Howler monkeys are the reservoir of malaria parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro

Abreu¹,

Santos

Mello

et al. 2019

Preprint

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BackgroundAlthough malaria transmission was eradicated from southeast Brazil, a significant increase in the number of Plasmodium vivax-like autochthonous human cases has been reported in remote areas of the Atlantic Forest in the last decades in Rio de Janeiro (RJ) state, including an outbreak in 2015-2016. The singular clinical and epidemiological aspects of several human cases combined with molecular and genetic data revealed that they were due to the non-human primate (NHP) parasite P. simium. The full understanding of the epidemiology of the autochthonous malaria in southeastern Brazil depends, however, upon the knowledge on the circulation of NHP Plasmodium in the foci and the determination of its reservoirs.MethodologyA large sampling effort was carried out in the Atlantic forest of RJ and its bordering states (Minas Gerais, São Paulo, Espírito Santo) for capture and examination of free-living NHPs. Blood and/or viscera were analyzed for Plasmodia infections through molecular and microscopic techniques.Principal findingsIn total, 146 NHPs of six species, from 30 counties in four states were tested. Howler monkeys (A. guariba clamitans) were the only NHP species found infected. In RJ, 26% of howlers were positive, among them 17% were found to be infected with P. simium. Importantly, specific single nucleotide polymorphisms were detected in all P. simium infected howlers regardless geographical origin of malaria foci. Interestingly, 71% of P. simium infected NHP were from the coastal slope of a mountain chain (Serra do Mar), where most human cases have been occurring. P. brasilianum/malariae was detected for the first time in 14% free-living howlers in RJ as well as in 25% of those from the Espírito Santo state. Moreover, malarial pigment was detected in spleen fragments of 50% of a subsample composed of howler monkeys found dead in both RJ and ES. All NHPs were negative for P. falciparum.Conclusions/SignificanceOur data indicate the howler monkeys as the main reservoir of the Atlantic forest human malaria in RJ and other sites in Southeast Brazil and reinforce its zoonotic nature.Author summaryThe present work consists of an unprecedented capture effort and large-scale field survey of plasmodial species in Non-human primates (NHPs) in RJ, a state recording a three-decade history of autochthonous human cases of benign tertian malaria pending epidemiological clarification of their origin. For the first time, we describe infection rates by Plasmodium sp.in free-living NHP, match the spatial distribution of P. simium in NHP with that of local human cases of benign tertian malaria due to this parasite, disclose howler monkeys as the only confirmed reservoir of this zoonotic malaria in the state and showed that specific single nucleotide polymorphisms were present in all P. simium infected howlers, regardless of the geographical origin of malaria foci. It is also the first time that P. brasilianum/malariae is recorded in free-living NHPs from Rio de Janeiro and the widespread distribution of this quartan-malaria parasite of zoonotic potential in the state is illustrated. Together, these findings increase the understanding about the simian malaria parasites in Atlantic Forests, as well as on the zoonotic character of autochthonous human malaria in Rio de Janeiro, providing subsidies for shaping surveillance and control.

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Section: Discussionmentioning

confidence: 78%

Howler monkeys are the reservoir of malaria parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro

Abreu¹,

Santos

Mello

et al. 2019

Preprint

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“…More recent studies using molecular techniques indicate a prevalence of 25 to 35 % in howler monkeys and a minimum infection rate of 0.01 to 1 % in An. cruzii [11,33,49,50,52,58,59]. A prevalence of around 2 to 3 % has been observed in human populations tested in areas of Southeastern Brazil [5][6][7].…”

Section: Discussionmentioning

confidence: 99%

A mathematical model for zoonotic transmission of malaria in the Atlantic Forest: exploring the effects of variations in vector abundance and acrodendrophily

Sousa

Laporta²,

Coutinho³

et al. 2020

Preprint

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Transmission foci of autochthonous malaria caused by Plasmodium vivax -like parasites have frequently been reported in the Atlantic Forest in Southeastern and Southern Brazil. Evidence suggests that malaria is a zoonosis in these areas as human infections by simian Plasmodium species have been detected, and the main vector of malaria in the Atlantic Forest, Anopheles ( Kerteszia ) cruzii , can blood feed on human and simian hosts. In view of the lack of models that seek to predict the dynamics of zoonotic transmission in this part of the Atlantic Forest, the present study proposes a new deterministic mathematical model that includes a transmission compartment for non-human primates and parameters that take into account vector displacement between the upper and lower forest strata. The effects of variations in the abundance and acrodendrophily of An. cruzii on the prevalence of infected humans in the study area and the basic reproduction number (R 0 ) for malaria were analyzed. The model parameters are based on the literature and fitting of the empirical data. Simulations performed with the model indicate that (1) an increase in the abundance of the vector in relation to the total number of blood-seeking mosquitoes leads to an asymptotic increase in both the proportion of infected individuals at steady state and R 0 ; (2) the proportion of infected humans at steady state is higher when displacement of the vector mosquito between the forest strata increases; and (3) in most scenarios, Plasmodium transmission cannot be sustained only between mosquitoes and humans, which implies that non-human primates play an important role in maintaining the transmission cycle. The proposed model contributes to a better understanding of the dynamics of malaria transmission in the Atlantic Forest.

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“…Non‐human primate health can be affected by the aetiological agents of malaria, even resulting in the death of some animals (Carvalho et al, ; Costa et al, ; Ozwara et al, ). In the present study, P. falciparum was detected for the first time in a specimen of S. bicolor classified as endangered on the IUCN Red List (IUCN, ).…”

Section: Discussionmentioning

confidence: 99%

“…Aetiological agents of simian malaria, such as P. brasilianum and P. simium , have also been diagnosed in Neotropical primates in Brazil (Alvarenga et al, , ; Arruda, ; Deane, ). Although NHPs are considered reservoirs of Plasmodium spp., these primates may present clinical symptoms similar to those seen in human malaria, such as fever, lethargy, apathy, dyspnoea, and cerebral compromise (Costa et al, ; Ibiwoye, Howard, Sibbons, Hasan, & Van Velzen, ; Ozwara et al, ). Additionally, it is important that such infections are identified in NHPs before translocation and reintroduction processes, as it may reduce the risk of Plasmodium spp.…”

Section: Introductionmentioning

confidence: 99%

“…The aetiological agents of human malaria also infect NHP and these mammals can act as reservoirs in different Brazilian biomes, which may have implications for public health (Araújo et al, ; Duarte et al, ; Costa et al, ; Figueiredo, Di Santini, Figueiredo, & Machado, ; Yamasaki et al,). Aetiological agents of simian malaria, such as P. brasilianum and P. simium , have also been diagnosed in Neotropical primates in Brazil (Alvarenga et al, , ; Arruda, ; Deane, ).…”

Section: Introductionmentioning

confidence: 99%

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Plasmodium vivax and Plasmodium falciparum infection in Neotropical primates in the western Amazon, Brazil

Silva

Barros

Bahia

et al. 2019

Zoonoses and Public Health

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The Brazilian Amazon is endemic for malaria and natural infections by Plasmodium spp. have been detected in Neotropical primates. Despite the diversity of primate species in the region, studies on infections by these agents are limited. The aim of the present study was to investigate the frequency of infection by Plasmodium vivax and P. falciparum in free‐born primates that were kept in captivity, in the western Amazon, Brazil. Blood samples were collected from 98 Neotropical primates. Detection of P. vivax and P. falciparum DNA was performed using a semi‐nested PCR, and the amplified products were sequenced. Plasmodium spp. DNA was detected in 6.12% (6/98) of the primates. P. vivax, and P. falciparum DNA was detected in 2.04% (2/98) and 4.08% (4/98) of these mammals, respectively. Sequencing and phylogenetic analysis confirmed the results obtained from the semi‐nested PCR. The presence of infected non‐human primates (NHP) can be auxiliary in the maintenance of P. falciparum and P. vivax and may have implications for the malaria surveillance and control in the Brazilian Amazon. It is necessary to structure an efficient surveillance system for the aetiological agents of malaria that infect NHP and humans to reduce the risk of Plasmodium spp. introduction into new areas, to protect all susceptible species.

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Plasmodium simium/Plasmodium vivax infections in southern brown howler monkeys from the Atlantic Forest

Cited by 27 publications

References 19 publications

Howler monkeys are the reservoir of malaria parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro

Howler monkeys are the reservoir of malaria parasites causing zoonotic infections in the Atlantic forest of Rio de Janeiro

A mathematical model for zoonotic transmission of malaria in the Atlantic Forest: exploring the effects of variations in vector abundance and acrodendrophily

Plasmodium vivax and Plasmodium falciparum infection in Neotropical primates in the western Amazon, Brazil

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