Socioecological vulnerability and the risk of zoonotic disease emergence in Brazil.

In developing countries, outbreaks of zoonotic diseases (ZDs) result from intertwined ecological, socioeconomic, and demographic processes that shape conditions for (i) increased contact between vulnerable human population and wildlife in areas undergoing environmental degradation and (ii) the rapid geographic spread of infections across socially vulnerable regions. In Brazil, recent increases in environmental and social vulnerabilities, amplified by economic and political crises, are potential triggers for outbreaks. We discuss Brazilian features that favor outbreaks and show a novel quantitative method for zoonotic risk assessment. Using data on nine ZDs from 2001 to 2019, we found that the most significant causal variables were vegetation cover and city remoteness. Furthermore, 8 of 27 states presented low-level risk of ZD outbreaks. Given the ZD-bushmeat connection, we identified central hunted mammals that should be surveilled to prevent spillover events. The current challenge is to coordinate intersectoral collaboration for effective One Health management in megadiverse countries with high social vulnerability and growing environmental degradation like Brazil.

Plasmodium simium: Population Genomics Reveals the Origin of a Reverse Zoonosis.

BACKGROUND: The population history of Plasmodium simium, which causes malaria in sylvatic Neotropical monkeys and humans along the Atlantic Coast of Brazil, remains disputed. Genetically diverse P vivax populations from various sources, including the lineages that founded the species P simium, are thought to have arrived in the Americas in separate migratory waves. METHODS: We use population genomic approaches to investigate the origin and evolution of P simium. RESULTS: We find a minimal genome-level differentiation between P simium and present-day New World P vivax isolates, consistent with their common geographic origin and subsequent divergence on this continent. The meagre genetic diversity in P simium samples from humans and monkeys implies a recent transfer from humans to non-human primates - a unique example of malaria as a reverse zoonosis of public health significance. Likely genomic signatures of P simium adaptation to new hosts include the deletion of >40% of a key erythrocyte invasion ligand, PvRBP2a, which may have favored more efficient simian host cell infection. CONCLUSIONS: New World P vivax lineages that switched from humans to platyrrhine monkeys founded the P simium population that infects nonhuman primates and feeds sustained human malaria transmission in the outskirts of major cities.

Ticks (Parasitiformes: Ixodida) on new world wild primates in Brazil

Brazil concentrates the largest number of primate species in the world. In the present study, an extensive literature review of ticks on New World wild monkeys has been carried out, demonstrating that between the years 1912 to 2018, 182 larvae, 137 nymphs and 31 adult ticks (10 males and 21 females) were collected on 78 primates (from 12 different species) in 28 distinct localities in the Brazilian territory. Additionally, examination of allotments of 11 tick collections of Brazil revealed that from 1919 to 2019, 93 larvae, 91 nymphs and 175 adult ticks (62 males and 113 females) were collected from 100 monkeys (among 20 different species) from 43 localities in distinct Brazilian biomes. Overall, 19 tick species were identified on wild primates in the country: Amblyomma aureolatum (Pallas, 1772), Amblyomma cajennense (Fabricius, 1787) sensu stricto, Amblyomma coelebs Neumann, 1899, Amblyomma dubitatum Neumann, 1899, Amblyomma geayi Neumann, 1899, Amblyomma incisum Neumann, 1906, Amblyomma longirostre (Koch, 1844), Amblyomma naponense (Packard, 1869), Amblyomma nodosum Neumann, 1899, Amblyomma ovale Koch, 1844, Amblyomma parkeri Fonseca & Aragão, 1952, Amblyomma romarioi Martins, Luz & Labruna, 2019, Amblyomma rotundatum Koch, 1844, Amblyomma sculptum Berlese, 1888, Haemaphysalis juxtakochi Cooley, 1946, Ixodes fuscipes Koch, 1844, Rhipicephalus microplus (Canestrini, 1888), Rhipicephalus sanguineus (Latreille, 1806) sensu lato,and Ornithodoros rostratus Aragão, 1911. The presence of A. incisum, A. naponense, A. nodosum, A. rotundatum and I. fuscipes on monkeys is recorded for the first time. Thisresearch is therefore a significant contribution to the knowledge of tick speciesassociated with non-human primates in the Neotropical region.

Spontaneous meningoencephalitis by Staphylococcus aureus in an infant golden-headed lion tamarin (Leontopithecus chrysomelas).

Non-human primates are susceptible to many bacteria, some of which bear zoonotic potential. We report the pathologic features of spontaneous fulminating meningoencephalitis by Staphylococcus aureus in a captive infant golden-headed lion tamarin (Leontopithecus chrysomelas) from Brazil.

Leptospira spp., rotavirus, norovirus, and hepatitis E virus surveillance in a wild invasive golden-headed lion tamarin (Leontopithecus chrysomelas; Kuhl, 1820) population from an urban park in Niterói, Rio de Janeiro, Brazil.

The world currently faces severe biodiversity losses caused by anthropogenic activities such as deforestation, pollution, the introduction of exotic species, habitat fragmentation, and climate changes. Disease ecology in altered environments is still poorly understood. The golden-headed lion tamarin (GHLT, Leontopithecus chrysomelas) is an endangered species that became invasive in an urban park in Niterói, Rio de Janeiro, Brazil. The initially few invasive GHLT individuals became hundreds, adapted to living in proximity to humans and domestic animals. These GHLTs were captured as part of a conservation project; some animals were translocated to Bahia and some were kept in captivity. This study tested 593 GHLT for Leptospira serology; 100 and 95 GHLT for polymerase chain reaction (PCR) toLeptospira and hepatitis E virus genotype 3 (HEV-3), respectively, and 101 familiar groups for PCR to viruses (rotavirus A, norovirus GI and GII, and HEV-3). One animal had antibodies for Leptospira serovar Shermani and another for serovar Hebdomadis. One saprophyticLeptospira was found by the 16S PCR and sequencing. Viruses were not detected in samples tested. Findings suggest that the epidemiological importance of such pathogens in this GHLT population is either low or nonexistent. These data are important to understand the local disease ecology, as well as monitoring a translocation project, and to contribute data for species conservation.

Spontaneous retroperitoneal liposarcoma in a free-ranging juvenile golden-headed lion tamarin (Leontopithecus chrysomelas).

Malignant adipocytic neoplasia is rare among nonhuman primates. We report the gross and microscopic features of a retroperitoneal liposarcoma with myxofibrosarcoma-like dedifferentiation in a free-ranging juvenile golden-headed lion tamarin (Leontopithecus chrysomelas). To our knowledge, this is the first report of such tumor subtype in New World primates.

Human migration and the spread of malaria parasites to the New World.

We examined the mitogenomes of a large global collection of human malaria parasites to explore how and when Plasmodium falciparum and P. vivax entered the Americas. We found evidence of a significant contribution of African and South Asian lineages to present-day New World malaria parasites with additional P. vivax lineages appearing to originate from Melanesia that were putatively carried by the Australasian peoples who contributed genes to Native Americans. Importantly, mitochondrial lineages of the P. vivax-like species P. simium are shared by platyrrhine monkeys and humans in the Atlantic Forest ecosystem, but not across the Amazon, which most likely resulted from one or a few recent human-to-monkey transfers. While enslaved Africans were likely the main carriers of P. falciparum mitochondrial lineages into the Americas after the conquest, additional parasites carried by Australasian peoples in pre-Columbian times may have contributed to the extensive diversity of extant local populations of P. vivax.

Evaluation of three chemical immobilization protocols in golden-headed lion tamarins (Leontopithecus chrysomelas) undergoing vasectomy surgery.

BACKGROUND: The golden-headed lion tamarin (Leontopithecus chrysomelas), originally endemic to Bahia, was introduced in Rio de Janeiro. The species is currently found in remaining forests within the region of original occupation of the golden lion tamarin (Leontopithecus rosalia), which may compromise the survival of the golden lion tamarin. Groups of golden-headed lion tamarins were captured and translocated to Bahia. However, the area chosen reached its limit and males underwent to vasectomy procedures. METHODS: Animals were separated into 3 groups: S-ketamine and midazolam, S-ketamine and dexmedetomidine, and racemic ketamine and dexmedetomidine. RESULTS AND CONCLUSIONS: Heart rate, sedation and muscle relaxation degrees, antinociception, and lidocaine consumption presented significant difference between midazolam and dexmedetomidine groups. Bradycardia was present on dexmedetomidine groups, with values remaining within the normal range. Dexmedetomidine groups present the best outcomes for muscle relaxation, sedation, and antinociception and were safe for vasectomy surgery in golden-headed lion tamarins.

Survey of Malassezia sp and dermatophytes in the cutaneous microbiome of free-ranging golden-headed lion tamarins (Leontopithecus chrysomelas - Kuhl, 1820).

BACKGROUND: Data about the presence of fungi on the cutaneous surface of wild animals are scarce. The aim of this study was to survey dermatophytes and Malassezia sp in the external ear canal and haircoat of Leontopithecus chrysomelas. METHODS: A total of 928 clinical samples were collected from 232 animals: For Malassezia screening 696 samples were studied, 464 of cerumen and 232 of haircoat; another 232 haircoat samples were studied for dermatophyte analysis. RESULTS: A geophilic dermatophyte, Microsporum cookie, was isolated from one young female. Lipodependent Malassezia was isolated from 76 animals and 87 clinical samples, 26 from the cerumen and 61 from the haircoat (statistically significant); there were no differences related to gender and age. CONCLUSIONS: Results suggested that lipodependent Malassezia is part of the skin microbiome of these animals. The prevalence of dermatophytes was too low and probably not relevant for the health of the studied population.

Merozoite surface protein-1 genetic diversity in Plasmodium malariae and Plasmodium brasilianum from Brazil.

BACKGROUND: The merozoite surface protein 1 (MSP1) gene encodes the major surface antigen of invasive forms of the Plasmodium erythrocytic stages and is considered a candidate vaccine antigen against malaria. Due to its polymorphisms, MSP1 is also useful for strain discrimination and consists of a good genetic marker. Sequence diversity in MSP1 has been analyzed in field isolates of three human parasites: P. falciparum, P. vivax, and P. ovale. However, the extent of variation in another human parasite, P. malariae, remains unknown. This parasite shows widespread, uneven distribution in tropical and subtropical regions throughout South America, Asia, and Africa. Interestingly, it is genetically indistinguishable from P. brasilianum, a parasite known to infect New World monkeys in Central and South America. METHODS: Specific fragments (1 to 5) covering 60 % of the MSP1 gene (mainly the putatively polymorphic regions), were amplified by PCR in isolates of P. malariae and P. brasilianum from different geographic origin and hosts. Sequencing of the PCR-amplified products or cloned PCR fragments was performed and the sequences were used to construct a phylogenetic tree by the maximum likelihood method. Data were computed to give insights into the evolutionary and phylogenetic relationships of these parasites. RESULTS: Except for fragment 4, sequences from all other fragments consisted of unpublished sequences. The most polymorphic gene region was fragment 2, and in samples where this region lacks polymorphism, all other regions are also identical. The low variability of the P. malariae msp1 sequences of these isolates and the identification of the same haplotype in those collected many years apart at different locations is compatible with a low transmission rate. We also found greater diversity among P. brasilianum isolates compared with P. malariae ones. Lastly, the sequences were segregated according to their geographic origins and hosts, showing a strong genetic and geographic structure. CONCLUSIONS: Our data show that there is a low level of sequence diversity and a possible absence of allelic dimorphism of MSP1 in these parasites as opposed to other Plasmodium species. P. brasilianum strains apparently show greater divergence in comparison to P. malariae, thus P. malariae could derive from P. brasilianum, as it has been proposed.

Pneumonia and bacteremia in a golden-headed lion tamarin (Leontopithecus chrysomelas) caused by Klebsiella pneumoniae subsp. pneumoniae during a translocation program of free-ranging animals in Brazil.

Klebsiella pneumoniae is an important emerging pathogen in humans, particularly the invasive hypermucoviscosity (HMV) phenotype. In addition, the organism is an important public health concern because of nosocomial infections and antimicrobial resistance. Nonhuman primates in captivity are susceptible to Klebsiella, particularly when a stress factor is involved. Infections vary depending on the species but can cause significant morbidity and mortality in these animals. The objective of this study was to describe a case of bronchopneumonia and bacteremia caused by Klebsiella pneumoniae in a free-ranging golden-headed lion tamarin (Leontopithecus chrysomelas) caught and maintained in quarantine during a translocation program for conservation purposes. An adult male, that had showed emaciation and apathy, was clinically examined and, despite being provided supportive therapy, died 2 days after onset of clinical signs. At postmortem examination, generalized bilateral pneumonia and pericarditis were observed. Tissue samples were fixed in 10% formalin for histology, and pulmonary tissues and cardiac blood were collected for microbiologic diagnostic procedures. Bacteria that were shown to be HMV K. pneumoniae subsp. pneumoniae strains were isolated from the pulmonary fluids and cardiac blood in pure cultures. Severe bronchopneumonia was the main pathological finding. The consequences of the confirmed presence of the HMV phenotype of K. pneumoniae subsp. pneumoniae in this wildlife species for human, animal, and ecosystem health should be determined. These results demonstrate the importance of quarantine and potential pathogen screening during wildlife translocation procedures.

Survey of Plasmodium spp. in free-ranging neotropical primates from the Brazilian Amazon region impacted by anthropogenic actions.

This study investigated Plasmodium spp. infection in free-ranging neotropical primates from Brazilian Amazon regions under the impact of major anthropogenic actions. Blood samples from 19 new world primates were collected and analyzed with microscopic and molecular procedures. The prevalence of Plasmodium infection was 21.0% (4/19) and PCR positive samples were identified as P. brasilianum. Considering the social-economic changes that the Amazon is facing, the prevalence of P. brasilianum infection highlights the necessity to closely monitor the movement of both human and non-human primate populations, in order to mitigate pathogen exposure and the introduction of new agents into previously naïve areas.