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Free-ranging nonhuman primates are frequent sources of zoonotic pathogens due to their physiologic similarity and in many tropical regions, close contact with humans. Many high-risk disease transmission interfaces have not been monitored for zoonotic pathogens due to difficulties inherent to invasive sampling of free-ranging wildlife. Non-invasive surveillance of nonhuman primates for pathogens with high potential for spillover into humans is therefore critical for understanding disease ecology of existing zoonotic pathogen burdens and identifying communities where zoonotic diseases are likely to emerge in the future. We developed a non-invasive oral sampling technique using ropes distributed to nonhuman primates to target viruses shed in the oral cavity, which through bite wounds and discarded food, could be transmitted to people. Optimization was performed by testing paired rope and oral swabs from laboratory colony rhesus macaques for rhesus cytomegalovirus (RhCMV) and simian foamy virus (SFV) and implementing the technique with free-ranging terrestrial and arboreal nonhuman primate species in Uganda and Nepal. Both ubiquitous DNA and RNA viruses, RhCMV and SFV, were detected in oral samples collected from ropes distributed to laboratory colony macaques and SFV was detected in free-ranging macaques and olive baboons. Our study describes a technique that can be used for disease surveillance in free-ranging nonhuman primates and, potentially, other wildlife species when invasive sampling techniques may not be feasible.

Background: Infectious diseases represent the greatest threats to endangered species, and transmission from humans to wildlife under increased anthropogenic pressure has been always stated as a major risk of habituation., Aims: To evaluate the impact of close contact with humans on the occurrence of potentially zoonotic protists in great apes, one hundred mountain gorillas (Gorilla beringei beringei) from seven groups habituated either for tourism or for research in Volcanoes National Park, Rwanda were screened for the presence of microsporidia, Cryptosporidium spp. and Giardia spp. using molecular diagnostics., Results: The most frequently detected parasites were Enterocytozoon bieneusi found in 18 samples (including genotype EbpA, D, C, gorilla 2 and five novel genotypes gorilla 4-8) and Encephalitozoon cuniculi with genotype II being more prevalent (10 cases) compared to genotype I (1 case). Cryptosporidium muris (2 cases) and C. meleagridis (2 cases) were documented in great apes for the first time. Cryptosporidium sp. infections were identified only in research groups and occurrence of E. cuniculi in research groups was significantly higher in comparison to tourist groups. No difference in prevalence of E. bieneusi was observed between research and tourist groups., Conclusion: Although our data showed the presence and diversity of important opportunistic protists in Volcanoes gorillas, the source and the routes of the circulation remain unknown. Repeated individual sampling, broad sampling of other hosts sharing the habitat with gorillas and quantification of studied protists would be necessary to acquire more complex data.

To facilitate ecotourism and research, free-ranging mountain gorillas of Uganda have been habituated to humans. Testing of fecal samples of gorillas (n = 100), people sharing gorilla habitats (n = 62). and local pre- and postweaned cattle (n = 50) having access to these habitats with fluorescein isothiocyanate-conjugated monoclonal antibodies revealed Giardia duodenalis cysts at prevalences of 2, 5, and 10%, respectively. The identification of G. duodenalis was confirmed by fluorescent in situ hybridization with 2 species-specific 18-bp oligonucleotide probes conjugated to hexachlorinated 6-carboxyfluorescein. The mean pathogen concentration was 2.5, 2.8, and 0.2 x 10(4) cysts/g of the gorilla, people, and cattle feces, respectively. All cyst isolates aligned with genotype (assemblage) A, as confirmed by polymerase chain reaction amplification and sequencing of a 130-bp region near the 5' end of the small subunit-ribosomal RNA gene. A single genotype (assemblage) A recovered from 3 genetically distant but geographically united host groups indicates anthropozoonotic transmission of G. duodenalis. A large percentage of the local community does not follow park regulations regarding the disposal of their fecal waste, as self-reported in a questionnaire. This genotype may have been introduced into gorilla populations through habituation activities and may have then been sustained in their habitats by anthropozoonotic transmission.

Cryptosporidiosis, a zoonotic diarrheal disease, significantly contributes to the mortality of people with impaired immune systems worldwide. Infections with an animal-adapted genotype (Genotype 2) of Cryptosporidium parvum were found in a human population in Uganda that shares habitats with free-ranging gorillas, from which the same genotype of C. parvum had been recovered previously. A high prevalence of disease was found in park staff members (21%) who frequently contact gorillas versus 3% disease prevalence in the local community. This indicates a zoonotic transmission cycle of this pathogen against which no effective prophylaxis or therapy exists. The results of the study questionnaire demonstrated a high percentage of people not undertaking appropriate precautions to prevent fecal-oral transmission of C. parvum in the Bwindi Impenetrable National Park, Uganda. This human population will benefit from stronger compliance with park regulations regarding disposal of their fecal waste within the park boundaries.

BackgroundHuman and filovirus host interactions remain poorly understood in areas where Ebola hemorrhagic fever outbreaks are likely to occur. In the Bwindi region of Uganda, a hot spot of mammalian biodiversity in Africa, human livelihoods are intimately connected with wildlife, creating potential for exposure to filoviruses.MethodsWe tested samples from 331 febrile patients presenting to healthcare facilities near Bwindi Impenetrable Forest, Uganda, by polymerase chain reaction (PCR) analysis and Western blot, using recombinant glycoprotein antigens for Ebola virus (EBOV), Sudan virus (SUDV), Bundibugyo virus (BDBV), and Marburg virus. Behavioral data on contact with wildlife were collected to examine risk factors for filovirus seropositivity.ResultsAll patients were negative for active filovirus infection, by PCR analysis. However, patients were seroreactive to SUDV (4.7%), EBOV (5.3%), and BDBV (8.9%), indicating previous exposure. Touching duikers was the most significant risk factor associated with EBOV seropositivity, while hunting primates and touching and/or eating cane rats were significant risk factors for SUDV seropositivity.ConclusionsPeople in southwestern Uganda have suspected previous exposure to filoviruses, particularly those with a history of wildlife contact. Circulation of filoviruses in wild animals and subsequent spillover into humans could be more common than previously reported.

Infectious diseases have the potential to extirpate populations of great apes. As the interface between humans and great apes expands, zoonoses pose an increasingly severe threat to already endangered great ape populations. Despite recognition of the threat posed by human pathogens to great apes, health monitoring is only conducted for a small fraction of the world's wild great apes (and mostly those that are habituated) meaning that outbreaks of disease often go unrecognized and therefore unmitigated. This lack of surveillance (even in sites where capacity to conduct surveillance is present) is the most significant limiting factor in our ability to quickly detect and respond to emerging infectious diseases in great apes when they first appear. Accordingly, we must create a surveillance system that links disease outbreaks in humans and great apes in time and space, and enables veterinarians, clinicians, conservation managers, national decision makers, and the global health community to respond quickly to these events. Here, we review existing great ape health surveillance programs in African range habitats to identify successes, gaps, and challenges. We use these findings to argue that standardization of surveillance across sites and geographic scales, that monitors primate health in real‐time and generates early warnings of disease outbreaks, is an efficient, low‐cost step to conserve great ape populations. Such a surveillance program, which we call "Great Ape Health Watch" would lead to long‐term improvements in outbreak preparedness, prevention, detection, and response, while generating valuable data for epidemiological research and sustainable conservation planning. Standardized monitoring of great apes would also make it easier to integrate with human surveillance activities. This approach would empower local stakeholders to link wildlife and human health, allowing for near real‐time, bidirectional surveillance at the great ape‐human interface. Highlights: This study reviewed existing great ape health surveillance programs in Africa and Asia to identify successes and challenges, and highlight the need for a standardized approach to great ape health surveillance.We propose "Great Ape Health Watch"—an integrated, real‐time monitoring system for great ape and human health that would generate early warnings of disease outbreaks, as a cost‐efficient strategy to secure future great ape conservation.Integrated ape–human syndromic surveillance would not only provide continuity in outbreak preparedness and data collection, but also empower local stakeholders to link wildlife and human health for impactful conservation and healthcare provisions. [ABSTRACT FROM AUTHOR]