Systematic review and meta-analysis on seroprevalence of leptospirosis in non-human primates worldwide.

Leptospirosis is a zoonotic disease whose transmission is linked to multiple factors involving the interface between animals, humans, and the environment. This disease is of great importance for public health, as it profoundly affects the health aspects of the population and animals. Considering the importance of non-human primates in this epidemiological chain, the objective of this research was to conduct a systematic literature review with meta-analysis, providing information on leptospirosis in non-human primates (NHPs) and an update on the infection situation in Brazil and other countries. Thus, a search was performed in five databases, initially finding 3332 studies, of which 32 met the eligibility criteria and were used for the systematic review. According to them, the most prevalent serogroup in non-human primates was Icterohaemorrhagiae, which is adapted to rodents as primary hosts. A wide distribution of the infection was found in the regions of both wild and captive animals. Through meta-analysis, the seroprevalence rate of leptospirosis in non-human primates was 27.21% (CI 17.97-38.95%). Cochran's Q test (p < 0.01) identified heterogeneity between studies, classified as high by the Higgins and Thompson test (I2 = 92.4%). Therefore, seroepidemiological and Leptospira isolation studies in non-human primates are important to investigate and monitor the suspected impact of these species as maintainers or transmitters of the pathogen to humans and other wild and domestic animals, in addition to demonstrating the need for standardization related to control and prevention measures.

Diagnostic features of metastatic endometrioid carcinoma in a captive black-tufted marmoset (Callithrix penicillata).

A captive marmoset developed metastatic endometrioid carcinoma (EnC), a rare uterine tumor in non-human primates (NHPs). The neoplasm showed marked microscopical malignant and tubulopapillary aspects, immunopositivity for pan-cytokeratin, CK7, estrogen receptor, and a high mitotic index (Ki-67). These features may contribute to the diagnosis and therapeutics of EnC in NHPs.

Topography landmarks of the infraorbital, mandibular and mentual foramens of Saimiri collinsi (Osgood, 1916) for anesthetic access and blocks.

Due to events related to the urbanization process, specimens of Saimiri collinsi are often referred to veterinarians specializing in the treatment of wild animals. With these professionals and the oral health of this species in mind, we evaluated the skull and the exact location of the infraorbital, mentual and mandibular foramens, with the aim of supporting the anesthetic block for dental procedures in Saimiri collinsi. The infraorbital foramen was located in the maxillary bone and was arranged with one on each side, except in one individual, with a pair in each antimer. The mentual foramen was located in the diastema between the canine tooth and the lateral incisor. The mandibular foramen was located medially on the ramus of the mandible, close to the mandibular incisure. The distances between the foramina and the main reference points, were greater in females than in males (p < 0.05). For access purposes, in the foramens investigated we suggest using a Gingival Needle 30G 21 mm Short, positioned externally at 15º to the maxillary bone to access the infraorbital foramen. Externally, perpendicular to the chin, in the diastema between the lower lateral incisor tooth and the canine tooth, to approach the mentual foramen, and ventral to the edge of the mandibular body, at a 90º angle, to access the mandibular foramen.

Diversity of gastrointestinal parasites and molecular characterization of Giardia duodenalis in free-living and captive howler monkeys (Alouatta guariba clamitans) in southern Brazil.

Non-human primates (NHPs) are the group that most share infectious agents with humans due to their close taxonomic relationship. The southern brown howler monkeys (Alouatta guariba clamitans) are endemic primates from Brazil and Argentina's Atlantic Forest. This study aimed to investigate the presence of intestinal parasites in free-living (FL) and captive (CA) southern brown howler monkeys. Thirty-nine stool samples were collected in two areas in southern Brazil, 15 FL and 24 CA. Stool sediments obtained by centrifugal sedimentation technique were used for microscopic analysis and direct immunofluorescence assay and evaluated by molecular analysis through amplification and sequencing of TPI fragments. Intestinal parasites Giardia duodenalis, Cryptosporidium spp., and Trypanoxyuris minutus were detected at coproparasitological analysis. This is the first report of the presence of Cryptosporidium spp. in free-living howlers. The molecular characterization of G. duodenalis isolates indicated assemblage B for the first time found in free-living A. guariba clamitans. The high prevalence of G. duodenalis transmission in CA howler monkeys can be explained by direct contact with humans and frequent soil contact. The presence of a potentially zoonotic assemblage in these animals indicates that the process of fragmentation and cohabitation with humans and livestock affects the wildlife, thus indicating a need for eco-health measures.

The human malaria-Aotus monkey model: a historical perspective in antimalarial chemotherapy research at the Gorgas Memorial Laboratory-Panama.

The human malaria-Aotus monkey model has served the malaria research community since its inception in 1966 at the Gorgas Memorial Laboratory (GML) in Panama. Spanning over five decades, this model has been instrumental in evaluating the in vivo efficacy and pharmacokinetics of a wide array of candidate antimalarial drugs, whether used singly or in combination. The animal model could be infected with drug-resistant and susceptible Plasmodium falciparum and Plasmodium vivax strains that follow a characteristic and reproducible course of infection, remarkably like human untreated and treated infections. Over the years, the model has enabled the evaluation of several synthetic and semisynthetic endoperoxides, for instance, artelinic acid, artesunate, artemether, arteether, and artemisone. These compounds have been evaluated alone and in combination with long-acting partner drugs, commonly referred to as artemisinin-based combination therapies, which are recommended as first-line treatment against uncomplicated malaria. Further, the model has also supported the evaluation of the primaquine analog tafenoquine against blood stages of P. vivax, contributing to its progression to clinical trials and eventual approval. Besides, the P. falciparum/Aotus model at GML has also played a pivotal role in exploring the biology, immunology, and pathogenesis of malaria and in the characterization of drug-resistant P. falciparum and P. vivax strains. This minireview offers a historical overview of the most significant contributions made by the Panamanian owl monkey (Aotus lemurinus lemurinus) to malaria chemotherapy research.

Possible Spreading of SARS-CoV-2 from Humans to Captive Non-Human Primates in the Peruvian Amazon.

Human-to-animal transmission events of SARS-CoV-2 (Severe Acute Respiratory Syndrome Coronavirus 2) have been reported in both domestic and wild species worldwide. Despite the high rates of contagion and mortality during the COVID-19 (Coronavirus Diseases 2019) pandemic in Peru, no instances of natural virus infection have been documented in wild animals, particularly in the Amazonian regions where human-wildlife interactions are prevalent. In this study, we conducted a surveillance investigation using viral RNA sequencing of fecal samples collected from 76 captive and semi-captive non-human primates (NHPs) in the Loreto, Ucayali, and Madre de Dios regions between August 2022 and February 2023. We detected a segment of the RNA-dependent RNA polymerase (RdRp) gene of SARS-CoV-2 by metagenomic sequencing in a pooled fecal sample from captive white-fronted capuchins (Cebus unicolor) at a rescue center in Bello Horizonte, Ucayali. Phylogenetic analysis further confirmed that the retrieved partial sequence of the RdRp gene matched the SARS-CoV-2 genome. This study represents the first documented instance of molecular SARS-CoV-2 detection in NHPs in the Peruvian Amazon, underscoring the adverse impact of anthropic activities on the human-NHP interface and emphasizing the importance of ongoing surveillance for early detection and prediction of future emergence of new SARS-CoV-2 variants in animals.

Investigation of Yellow Fever Virus at the Human-Animal Interface after a Zika Virus Outbreak in Midwest Brazil.

Following the first report of zika virus in March 2015, Brazil experienced its largest sylvatic yellow fever outbreak between 2016 and 2019. This study aimed to investigate the circulation of yellow fever virus (YFV) in non-human primates (NHPs) and mosquitoes collected in urban parks and other metropolitan areas of midwest Brazil between 2017 and 2018. Whole blood samples from 80 NHPs, including 48 black-tailed marmosets (Mico melanurus) and 2332 mosquitoes from six different genera, were collected in the states of Mato Grosso (MT) and Mato Grosso do Sul (MS) and then tested for YFV by RT-qPCR. Additionally, 23 plasma samples of NHPs were tested for neutralizing antibodies for YFV by a plaque reduction neutralization test (PRNT). No YFV RNA or neutralizing antibodies for YFV were detected in NHPs and mosquitoes from MT and MS. The continuous monitoring of YFV circulation in different species of NHPs and vectors in urban areas is instrumental to quickly assess potentially unknown maintenance cycles of yellow fever at the human-animal interface in Brazil.

From imaging to precision: low cost and accurate determination of stereotactic coordinates for brain surgery Sapajus apella using MRI.

The capuchin monkey (Sapajus apella), a New World monkey species, exhibits prominent characteristics that make it an ideal model for neuroscience research. These characteristics include its phylogenetic traits, telencephalization coefficient, anatomical structures and pathways, genetic profile, immune responses, cognitive abilities, and complex behavioral repertoires. Traditionally, methodologies for stereotactic neurosurgery in research models have relied on the use of brain atlases. However, this approach can lead to errors due to the considerable variation in brain size and shape among individual monkeys. To address this issue, we developed a protocol for deriving individual coordinates for each monkey using a straightforward and relatively inexpensive method involving MRI imaging. Our protocol utilizes a specially designed, 3D-printed stereotactic head-holder that is safe to use with an MR magnet, non-invasive placement of fiducial markers, and post-processing with open-source software. This approach enhances MRI data visualization, improves anatomical targeting, and refines the design of neurosurgical experiments. Our technique could also prove beneficial in other areas of neuroscience research that require accurate calculation of stereotaxic coordinates. Furthermore, it could be useful for other nonhuman primate species for which brain atlases are typically unavailable.

Radiographically guided femoral neck osteosynthesis with cannulated compressive titanium screw and anti-rotational component in a Brown Howler Monkey (Alouatta guariba clamitans).

A Brown Howler Monkey presented with a femoral neck fracture was successfully treated with a cannulated compressive screw and an anti-rotational component inserted with radiographically guided technique. Complete bone consolidation and functional recovery were observed 9 weeks after the surgery, and the monkey was released to his place of origin.

Traumatic chylothorax in urbanized free-ranging black-tufted marmosets (Callithrix penicillata).

After fatal traumatic injuries, three urbanized free-ranging marmosets developed a milky white or pink-white thoracic alkaline effusion with high specific gravity, triglyceride levels, and predominance of small lymphocytes. Chylothorax is an uncommon thoracic fluid accumulation in animals and humans and has not been reported in free-ranging non-human primates.

Gastrointestinal Parasites Affecting Non-Human Primates That Are Kept Ex Situ and Their Handlers in Different Brazilian Institutions: Diagnosis and Analysis of Risk Factors.

AIM: Determining gastrointestinal parasites' frequency in non-human primates (NHPs) and handlers in different Brazilian institutions, and associate it with management information. METHODS: Different institutions in São Paulo (A), Brasília (B), Rio de Janeiro (C), Pará (D) and Santa Catarina (E) were included in the study. Fecal samples were processed by using coproparasitological techniques; information about NHP handling and professionals' routine were collected through the use of questionnaires. RESULTS: In total, 33.1% of 511 NHP samples were positive for parasites; the Entamoebidae Group and Strongyloides sp.-compatible eggs were the most detected protozoa and helminths, respectively. The Entamoebidae Group was mainly diagnosed in Alouatta from Institutions E and D, and was also the only parasite detected in handlers. Strongyloides-compatible eggs were mostly evident in fecal samples collected from Cebidae from Institutions B and D. Some risk factors associated with parasite infection were a high number of animals in the same enclosure and their use for research protocol purposes, whereas quarantine, a post-infection vacant period in enclosures and antiparasitic supply were categorized as protective factors against these agents' infection. CONCLUSIONS: Parasites showing different transmission routes but concomitantly circulating in NHP institutions located in different Brazilian regions were identified in the current study, with an emphasis on those presenting zoonotic potential.

Case report: Urbanized non-human primates as sentinels for human zoonotic diseases: a case of acute fatal toxoplasmosis in a free-ranging marmoset in coinfection with yellow fever virus.

Free-ranging non-human primates (NHP) can live in anthropized areas or urban environments in close contact with human populations. This condition can enable the emergence and transmission of high-impact zoonotic pathogens. For the first time, we detected a coinfection of the yellow fever (YF) virus with Toxoplasma gondii in a free-ranging NHP in a highly urbanized area of a metropolis in Brazil. Specifically, we observed this coinfection in a black-tufted marmoset found dead and taken for a necropsy by the local health surveillance service. After conducting an epidemiological investigation, characterizing the pathological features, and performing molecular assays, we confirmed that the marmoset developed an acute fatal infection caused by T. gondii in coinfection with a new YF virus South American-1 sub-lineage. As a result, we have raised concerns about the public health implications of these findings and discussed the importance of diagnosis and surveillance of zoonotic agents in urbanized NHPs. As competent hosts of zoonotic diseases such as YF and environmental sentinels for toxoplasmosis, NHPs play a crucial role in the One Health framework to predict and prevent the emergence of dangerous human pathogens.

Fatal Simplexvirus humanalpha1 infection in howler-monkeys (Alouatta sp.) under human care: Clinical, molecular, and pathological findings.

BACKGROUND: Simplexvirus humanalpha1 (HuAHV-1) are common anthropozoonosis reported in marmosets but rare in howler monkeys (Alouatta sp.). METHODS: Necropsy of two brown-howler monkeys (A. caraya) and one red-howler monkey (A. guariba clamitans) from different zoo collections were performed. Fragments of all organs were examined through microscopy. Samples were submitted to IHC for Simplexvirus humanalpha 2 (HuAHV-2) [sin. Herpesvirus simplex type 2] and PCR. RESULTS: Grossly, only the A. guariba showed liver lesions characterized by multifocal, pinpoint white areas corresponding microscopically as random necrotizing herpetic hepatitis and ulcerative glossitis. Both A. caraya showed necrotizing meningoencephalitis with Cowdry A-type body inclusions within neurons and astrocytes. Immunolabeling for HuAHV-1/2 was observed in the tongue, liver, and brain. HuAHV-1 was confirmed in all samples by PCR, Sanger sequencing, and phylogenetic analyses. CONCLUSION: Necrotizing meningoencephalitis was appreciated in 2/3 of animals, and it is associated with neurologic signs. Along with ulcerative glossitis, a hallmark lesion in marmosets, it was present in one animal. Regarding herpetic hepatitis, it is not frequent in monkeys and occurs mainly in immunocompromised animals. HuAHV-1 infection was confirmed corroborating with a human source. This is the second report on captive black-howler monkeys and the first gross, histologic, immunohistochemical, and molecular description of herpetic hepatitis and ulcerative glossitis in red-howler monkeys (A. guariba).

Concentrations of iron and chromium in free-ranging common marmosets (Callithrix jacchus) from Pernambuco, Brazil.

Common marmosets (Callithrix jacchus) are widely distributed in Northeast Brazil and often inhabit urban and peri-urban forest areas close to human settlements. Given its wide territorial distribution, its proximity to human populations, and its exposure to environmental degradations originating from urbanization, common marmosets have a high potential for environmental biomonitoring. The concentrations of iron (Fe) and chromium (Cr) were quantified in the liver, hair, and bone of 22 free-ranging common marmosets' bodies from nine cities from Pernambuco State, Brazil, using inductively coupled plasma optical emission spectrometry (ICP OES). The liver showed the highest concentrations of Fe and Cr (3773.2 ± 3715.8 mg/kg and 19.4 ± 41.6 mg/kg, respectively); the lowest concentration of Fe was detected in the bone (111.6 ± 97.6 mg/kg) and of Cr in the hair (3.3 ± 1.5 mg/kg). There was a moderate positive correlation between Fe and Cr in the liver (r = 0.64) and a high negative correlation for Cr between bone and hair (r = -0.65). This study demonstrated the bioaccumulation of Fe and Cr in hair, liver, and bone in common marmosets. The highest average concentration of Fe and Cr occurred in animals from Recife, Jaboatão dos Guararapes, and Paulista, respectively, the 1st, the 2nd, and the 5th most populated cities in the state of Pernambuco. The presence of high concentrations of metals in animals from Recife and nearby cities can indicate alarming levels of environmental pollution in these locations.

Hematological and serum biochemistry evaluation in howler monkeys (Alouatta caraya) and capuchin monkeys (Sapajus apella): A comparative study.

BACKGROUND: Evaluation of blood parameters in captive non-human primates (NHPs) is crucial for monitoring their health and ensuring that their environment meets their physiological requirements. METHODS: We performed hemogram, serum biochemistry, and parasitological exams in 20 howler monkeys and 21 capuchin monkeys. RESULTS: In both species, over 50% of the individuals presented at least one parasite. There was a negative effect of age on red blood cell (RBC), white blood cell, platelets, total protein, globulin, and alkaline phosphatase, and a positive effect on the A:G ratio, gamma-glutamyl transferase, and mean platelet volume (MPV). Capuchin monkeys presented the highest platelets and alanine aminotransferase (ALT) values and howler monkeys presented the highest MPV, aspartate aminotransferase, ALT, amylase, glucose, bilirubin, and triglycerides values. We observed an interaction between species and sex on RBC, Htc, mean corpuscular hemoglobin concentration, and cholesterol. CONCLUSIONS: Species differences found in blood parameters may reflect differences in physiological adaptations associated with ecological and morphological traits and are clinically relevant for evaluating animal health and the suitability of breeding programs.

Staphylococcus nasal colonization in three species of non-human primates.

Bacterial nasal colonization is common in many mammals and Staphylococcus represents the main pathogen isolated. Staphylococcus nasal carriage in humans constitutes a risk factor for Staphylococcus infections pointing out the need for animal experimentation for nasal colonization studies, especially for vaccine development. A limitation in addressing this hypothesis has been a lack of appropriate animal model. Murine models do not mimic human nasal colonization studies. Non-human primates (NHP) remain the best classical models for nasal colonization studies. In this study, we analyzed nasal colonization between two species of Old World monkeys (cynomolgus and rhesus) and a New World monkey (squirrel monkey) from breeding colony at Fiocruz (Brazil). Sixty male and female NHP with the average age of 1-21 years old, comprising twenty animals of each species, were analyzed. Nine different Staphylococcus species (S. aureus, S. cohnii, S. saprophyticus, S. haemolyticus, S. xylosus, S. warneri, S. nepalensis, S. simiae, and S. kloosi) were identified by MALDI-TOF and 16S rRNA gene sequence analyses. Antibiotic resistance was not detected among the isolated bacterial population. S. aureus was the main isolate (19 strains), present in all species, predominant in cynomolgus monkeys (9/20) and squirrel monkeys (7/20). spa typing was used to examine the clonal structure and genetic profile of Staphylococcus aureus isolates. Eight (8) spa types were identified among the S. aureus strains. A major cluster was identified, corresponding to a new spa type t20455, and no spa types found in this study were seen before in Brazil.

Arboviruses in Mammals in the Neotropics: A Systematic Review to Strengthen Epidemiological Monitoring Strategies and Conservation Medicine.

Arthropod-borne viruses (arboviruses) are a diverse group of ribonucleic acid (RNA) viruses, with the exception of African swine fever virus, that are transmitted by hematophagous arthropods to a vertebrate host. They are the important cause of many diseases due to their ability to spread in different environments and their diversity of vectors. Currently, there is no information on the geographical distribution of the diseases because the routes of transmission and the mammals (wild or domestic) that act as potential hosts are poorly documented or unknown. We conducted a systematic review from 1967 to 2021 to identify the diversity of arboviruses, the areas, and taxonomic groups that have been monitored, the prevalence of positive records, and the associated risk factors. We identified forty-three arboviruses in nine mammalian orders distributed in eleven countries. In Brazil, the order primates harbor the highest number of arbovirus records. The three most recorded arboviruses were Venezuelan equine encephalitis, Saint Louis encephalitis and West Nile virus. Serum is the most used sample to obtain arbovirus records. Deforestation is identified as the main risk factor for arbovirus transmission between different species and environments (an odds ratio of 1.46 with a 95% confidence interval: 1.34-1.59). The results show an increase in the sampling effort over the years in the neotropical region. Despite the importance of arboviruses for public health, little is known about the interaction of arboviruses, their hosts, and vectors, as some countries and mammalian orders have not yet been monitored. Long-term and constant monitoring allows focusing research on the analysis of the interrelationships and characteristics of each component animal, human, and their environment to understand the dynamics of the diseases and guide epidemiological surveillance and vector control programs. The biodiversity of the Neotropics should be considered to support epidemiological monitoring strategies.

Hepatitis E Virus Research in Brazil: Looking Back and Forwards.

Hepatitis E virus (HEV) has emerged as a public health concern in Brazil. From the first identification and characterization of porcine and human HEV-3 strains in the 2000s, new HEV subtypes have been identified from animal, human, and environmental isolates. As new potential animal reservoirs have emerged, there is a need to compile evidence on the zoonotic dissemination of the virus in animal hosts and the environment. The increasing amount of seroprevalence data on sampled and randomly selected populations must be systematically retrieved, interpreted, and considered under the One Health concept. This review focused on HEV seroprevalence data in distinct animal reservoirs and human populations reported in the last two decades. Furthermore, the expertise with experimental infection models using non-human primates may provide new insights into HEV pathogenesis, prevention, and environmental surveillance.

Prevalence of Platynosomum spp infection and its association with biliary lithiasis and secondary bacterial infections in free-ranging marmosets (Callithrix spp) of the Brazilian Atlantic Forest.

Platynosomosis is a parasitic disease caused by a trematode of the genus Platynosomum, a bile duct and gallbladder fluke that has been described in captive neotropical primates (New World primates; NWPs) and causes high morbidity and variable mortality. Although it is a major concern for ex-situ conservation of these animals, there are only a few studies of platynosomosis in free-ranging NWPs. Therefore, the aim of this study was to characterize platynosomosis in a free-ranging population of marmosets (Callithrix spp) from the Brazilian Atlantic Forest, focusing on the epidemiological and pathological aspects of the disease. A total of 1,001 marmosets were evaluated and on the basis of clinicoepidemiological data, histopathology, histochemistry and immunohistochemistry, we concluded that Platynosomum spp infection has a prevalence of 8.9% (confidence interval: 7.3-10.8%) in free-ranging marmosets, with a higher frequency in the Metropolitan Region of Rio de Janeiro. Infection was associated with fibrosing and proliferative cholangiohepatitis associated with biliary lithiasis (3.0% of cases) and secondary bacterial infections (14.6% of cases).

Genomic insights into ESBL-producing Escherichia coli isolated from non-human primates in the Peruvian Amazon.

Introduction: Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae are on the WHO priority pathogens list because they are associated with high mortality, health-care burden, and antimicrobial resistance (AMR), a serious problem that threatens global public health and should be addressed through the One Health approach. Non-human primates (NHP) have a high risk of acquiring these antibiotic-resistant bacteria due to their close phylogenetic relationship with humans and increased anthropogenic activities in their natural environments. This study aimed to detect and analyze the genomes of ESBL-producing Escherichia coli (ESBL-producing E. coli) in NHP from the Peruvian Amazon. Materials and methods: We collected a total of 119 fecal samples from semi-captive Saguinus labiatus, Saguinus mystax, and Saimiri boliviensis, and captive Ateles chamek, Cebus unicolor, Lagothrix lagothricha, and Sapajus apella in the Loreto and Ucayali regions, respectively. Subsequently, we isolated and identified E. coli strains by microbiological methods, detected ESBL-producing E. coli through antimicrobial susceptibility tests following CLSI guidelines, and analyzed their genomes using previously described genomic methods. Results: We detected that 7.07% (7/99) of E. coli strains: 5.45% (3/55) from Loreto and 9.09% (4/44) from Ucayali, expressed ESBL phenotype. Genomic analysis revealed the presence of high-risk pandemic clones, such as ST10 and ST117, carrying a broad resistome to relevant antibiotics, including three blaCTX-M variants: blaCTX-M-15, blaCTX-M-55, and blaCTX-M-65. Phylogenomic analysis confirmed the clonal relatedness of high-risk lineages circulating at the human-NHP interface. Additionally, two ESBL-producing E. coli strains were identified as EPEC (eae) and ExPEC according to their virulence profiles, and one more presented a hypermucoviscous phenotype. Discussion: We report the detection and genomic analysis of seven ESBL-producing E. coli strains carrying broad resistome and virulence factors in NHP from two regions of the Peruvian Amazon. Some of these strains are closely related to high-risk pandemic lineages previously reported in humans and domestic animals, highlighting the negative impact of anthropogenic activities on Amazonian wildlife. To our knowledge, this is the first documentation of ESBL-producing E. coli in NHP from the Amazon, underscoring the importance of adopting the One Health approach to AMR surveillance and minimizing the potential transmission risk of antibiotic-resistant bacteria at the human-NHP interface.