Higher convergence of human-great ape enteric eukaryotic viromes in central African forest than in a European zoo: a One Health analysis.

Human-animal pathogenic transmissions threaten both human and animal health, and the processes catalyzing zoonotic spillover and spillback are complex. Prior field studies offer partial insight into these processes but overlook animal ecologies and human perceptions and practices facilitating human-animal contact. Conducted in Cameroon and a European zoo, this integrative study elucidates these processes, incorporating metagenomic, historical, anthropological and great ape ecological analyses, and real-time evaluation of human-great ape contact types and frequencies. We find more enteric eukaryotic virome sharing between Cameroonian humans and great apes than in the zoo, virome convergence between Cameroonian humans and gorillas, and adenovirus and enterovirus taxa as most frequently shared between Cameroonian humans and great apes. Together with physical contact from hunting, meat handling and fecal exposure, overlapping human cultivation and gorilla pillaging in forest gardens help explain these findings. Our multidisciplinary study identifies environmental co-use as a complementary mechanism for viral sharing.

A multi-disciplinary comparison of great ape gut microbiota in a central African forest and European zoo.

Comparisons of mammalian gut microbiota across different environmental conditions shed light on the diversity and composition of gut bacteriome and suggest consequences for human and animal health. Gut bacteriome comparisons across different environments diverge in their results, showing no generalizable patterns linking habitat and dietary degradation with bacterial diversity. The challenge in drawing general conclusions from such studies lies in the broad terms describing diverse habitats ("wild", "captive", "pristine"). We conducted 16S ribosomal RNA gene sequencing to characterize intestinal microbiota of free-ranging sympatric chimpanzees and gorillas in southeastern Cameroon and sympatric chimpanzees and gorillas in a European zoo. We conducted participant-observation and semi-structured interviews among people living near these great apes to understand better their feeding habits and habitats. Unexpectedly, bacterial diversity (ASV, Faith PD and Shannon) was higher among zoo gorillas than among those in the Cameroonian forest, but zoo and Cameroonian chimpanzees showed no difference. Phylogeny was a strong driver of species-specific microbial composition. Surprisingly, zoo gorilla microbiota more closely resembled that of zoo chimpanzees than of Cameroonian gorillas. Zoo living conditions and dietary similarities may explain these results. We encourage multidisciplinary approach integrating environmental sampling and anthropological evaluation to characterize better diverse environmental conditions of such investigations.

Using physical contact heterogeneity and frequency to characterize dynamics of human exposure to nonhuman primate bodily fluids in central Africa.

Emerging infectious diseases of zoonotic origin constitute a recurrent threat to global health. Nonhuman primates (NHPs) occupy an important place in zoonotic spillovers (pathogenic transmissions from animals to humans), serving as reservoirs or amplifiers of multiple neglected tropical diseases, including viral hemorrhagic fevers and arboviruses, parasites and bacteria, as well as retroviruses (simian foamy virus, PTLV) that are pathogenic in human beings. Hunting and butchering studies in Africa characterize at-risk human social groups, but overlook critical factors of contact heterogeneity and frequency, NHP species differences, and meat processing practices. In southeastern Cameroon, a region with a history of zoonotic emergence and high risk of future spillovers, we conducted a novel mixed-method field study of human physical exposure to multiple NHP species, incorporating participant-based and ecological methodologies, and qualitative interviews (n = 25). We find frequent physical contact across adult human populations, greater physical contact with monkeys than apes, especially for meat handling practices, and positive correlation of human exposure with NHP species abundance and proximity to human settlement. These fine-grained results encourage reconsideration of the likely dynamics of human-NHP contact in past and future NTD emergence events. Multidisciplinary social science and ecological approaches should be mobilized to generate more effective human and animal surveillance and risk communications around neglected tropical diseases. At a moment when the WHO has included "Disease X", a presumably zoonotic pathogen with pandemic potential, on its list of blueprint priority diseases as, new field-based tools for investigating zoonotic disease emergence, both known and unknown, are of critical importance.

Rethinking Human-Nonhuman Primate Contact and Pathogenic Disease Spillover.

Zoonotic transmissions are a major global health risk, and human-animal contact is frequently raised as an important driver of transmission. A literature examining zooanthroponosis largely agrees that more human-animal contact leads to more risk. Yet the basis of this proposition, the term contact, has not been rigorously analyzed. To understand how contact is used to explain cross-species spillovers, we conducted a multi-disciplinary review of studies addressing human-nonhuman primate (NHP) engagements and pathogenic transmissions and employing the term contact. We find that although contact is frequently invoked, it is employed inconsistently and imprecisely across these studies, overlooking the range of pathogens and their transmission routes and directions. We also examine a related but more expansive approach focusing on human and NHP habitats and their spatial overlap, which can potentially facilitate pathogenic transmission. Contact and spatial overlap investigations cannot, however, explain the processes that bring together people, animals and pathogens. We therefore examine another approach that enhances our understanding of zoonotic spillovers: anthropological studies identifying such historical, social, environmental processes. Comparable to a One Health approach, our ongoing research in Cameroon draws contact, spatial overlap and anthropological-historical approaches into dialog to suggest where, when and how pathogenic transmissions between people and NHPs may occur. In conclusion, we call for zoonotic disease researchers to specify more precisely the human-animal contacts they investigate and to attend to how broader ecologies, societies and histories shape pathogen-human-animal interactions.

Beyond the Cut Hunter: A Historical Epidemiology of HIV Beginnings in Central Africa.

In the absence of direct evidence, an imagined "cut hunter" stands in for the index patient of pandemic HIV/AIDS. During the early years of colonial rule, this explanation goes, a hunter was cut or injured from hunting or butchering a chimpanzee infected with simian immunodeficiency virus, resulting in the first sustained human infection with the virus that would emerge as HIV-1M. We argue here that the "cut hunter" relies on a historical misunderstanding and ecological oversimplification of human-chimpanzee (Pan Troglodytes troglodytes) interactions that facilitated pathogenic transmission. This initial host shift cannot explain the beginnings of the HIV/AIDS pandemic. Instead, we must understand the processes by which the virus became transmissible, possibly between Sangha basin inhabitants and ultimately reached Kinshasa. A historical epidemiology of the late nineteenth and twentieth centuries, provides a much-needed corrective to the major shortcomings of the cut hunter. Based on 62 oral historical interviews conducted in southeastern Cameroon and archival research, we show that HIV emerged from ecological, economic, and socio-political transformations of the late nineteenth and twentieth centuries. The gradual imposition of colonial rule built on and reoriented ecologies and economies, and altered older patterns of mobility and sociality. Certain changes may have contributed to the initial viral host shift, but more importantly, facilitated the adaptation of HIV-1M to human-to-human transmission. Our evidence suggests that the most critical changes occurred after 1920. This argument has important implications for public health policy, underscoring recent work emphasizing alternative pathways for zoonotic spillovers into human beings.