Diversity and prevalence of zoonotic infections at the animal-human interface of primate trafficking in Peru

Wildlife trafficking creates favorable scenarios for intra- and inter-specific interactions that can lead to parasite spread and disease emergence. Among the fauna affected by this activity, primates are relevant due to their potential to acquire and share zoonoses - infections caused by parasites that can spread between humans and other animals. Though it is known that most primate parasites can affect multiple hosts and that many are zoonotic, comparative studies across different contexts for animal-human interactions are scarce. We conducted a multi-parasite screening targeting the detection of zoonotic infections in wild-caught monkeys in nine Peruvian cities across three contexts: captivity (zoos and rescue centers, n = 187); pet (households, n = 69); and trade (trafficked or recently confiscated, n = 132). We detected 32 parasite taxa including mycobacteria, simian foamyvirus, bacteria, helminths, and protozoa. Monkeys in the trade context had the highest prevalence of hemoparasites (including Plasmodium malariae/brasilianum, Trypanosoma cruzi, and microfilaria) and enteric helminths and protozoa were less common in pet monkeys. However, parasite communities showed overall low variation between the three contexts. Parasite richness (PR) was best explained by host genus and the city where the animal was sampled. Squirrel (genus Saimiri) and wooly (genus Lagothrix) monkeys had the highest PR, which was ~2.2 times the PR found in tufted capuchins (genus Sapajus) and tamarins (genus Saguinus/Leontocebus) in a multivariable model adjusted for context, sex, and age. Our findings illustrate that the threats of wildlife trafficking to One Health encompass exposure to multiple zoonotic parasites well-known to cause disease in humans, monkeys, and other species. We demonstrate these threats continue beyond the markets where wildlife is initially sold; monkeys trafficked for the pet market remain a reservoir for and contribute to the translocation of zoonotic parasites to households and other captive facilities where contact with humans is frequent. Our results have practical applications for the healthcare of rescued monkeys and call for urgent action against wildlife trafficking and ownership of monkeys as pets

Socializing One Health: an innovative strategy to investigate social and behavioral risks of emerging viral threats

In an effort to strengthen global capacity to prevent, detect, and control infectious diseases in animals and people, the United States Agency for International Development’s (USAID) Emerging Pandemic Threats (EPT) PREDICT project funded development of regional, national, and local One Health capacities for early disease detection, rapid response, disease control, and risk reduction. From the outset, the EPT approach was inclusive of social science research methods designed to understand the contexts and behaviors of communities living and working at human-animal-environment interfaces considered high-risk for virus emergence. Using qualitative and quantitative approaches, PREDICT behavioral research aimed to identify and assess a range of socio-cultural behaviors that could be influential in zoonotic disease emergence, amplification, and transmission. This broad approach to behavioral risk characterization enabled us to identify and characterize human activities that could be linked to the transmission dynamics of new and emerging viruses. This paper provides a discussion of implementation of a social science approach within a zoonotic surveillance framework. We conducted in-depth ethnographic interviews and focus groups to better understand the individual- and community-level knowledge, attitudes, and practices that potentially put participants at risk for zoonotic disease transmission from the animals they live and work with, across 6 interface domains. When we asked highly-exposed individuals (ie. bushmeat hunters, wildlife or guano farmers) about the risk they perceived in their occupational activities, most did not perceive it to be risky, whether because it was normalized by years (or generations) of doing such an activity, or due to lack of information about potential risks. Integrating the social sciences allows investigations of the specific human activities that are hypothesized to drive disease emergence, amplification, and transmission, in order to better substantiate behavioral disease drivers, along with the social dimensions of infection and transmission dynamics. Understanding these dynamics is critical to achieving health security--the protection from threats to health-- which requires investments in both collective and individual health security. Involving behavioral sciences into zoonotic disease surveillance allowed us to push toward fuller community integration and engagement and toward dialogue and implementation of recommendations for disease prevention and improved health security

The impact of the COVID-19 pandemic on rabies reemergence in Latin America: The case of Arequipa, Peru.

In Latin America, there has been tremendous progress towards eliminating canine rabies. Major components of rabies elimination programs leading to these successes have been constant and regular surveillance for rabid dogs and uninterrupted yearly mass dog vaccination campaigns. Unfortunately, vital measures to control COVID-19 have had the negative trade-off of jeopardizing these rabies elimination and prevention activities. We aimed to assess the effect of interrupting canine rabies surveillance and mass dog vaccination campaigns on rabies trends. We built a deterministic compartment model of dog rabies dynamics to create a conceptual framework for how different disruptions may affect rabies virus transmission. We parameterized the model for conditions found in Arequipa, Peru, a city with active rabies virus transmission. We examined our results over a range of plausible values for R0 (1.36-2.0). Also, we prospectively evaluated surveillance data during the pandemic to detect temporal changes. Our model suggests that a decrease in canine vaccination coverage as well as decreased surveillance could lead to a sharp rise in canine rabies within months. These results were consistent over all plausible values of R0. Surveillance data from late 2020 and early 2021 confirms that in Arequipa, Peru, rabies cases are on an increasing trajectory. The rising rabies trends in Arequipa, if indicative to the region as whole, suggest that the achievements made in Latin America towards the elimination of dog-mediated human rabies may be in jeopardy

Socio-spatial heterogeneity in participation in mass dog rabies vaccination campaigns, Arequipa, Peru.

To control and prevent rabies in Latin America, mass dog vaccination campaigns (MDVC) are implemented mainly through fixed-location vaccination points: owners have to bring their dogs to the vaccination points where they receive the vaccination free of charge. Dog rabies is still endemic in some Latin-American countries and high overall dog vaccination coverage and even distribution of vaccinated dogs are desired attributes of MDVC to halt rabies virus transmission. In Arequipa, Peru, we conducted a door-to-door post-campaign survey on >6,000 houses to assess the placement of vaccination points on these two attributes. We found that the odds of participating in the campaign decreased by 16% for every 100 m from the owner's house to the nearest vaccination point (p = 0.041) after controlling for potential covariates. We found social determinants associated with participating in the MDVC: for each child under 5 in the household, the odds of participating in the MDVC decreased by 13% (p = 0.032), and for each decade less lived in the area, the odds of participating in the MDVC decreased by 8% (p<0.001), after controlling for distance and other covariates. We also found significant spatial clustering of unvaccinated dogs over 500 m from the vaccination points, which created pockets of unvaccinated dogs that may sustain rabies virus transmission. Understanding the barriers to dog owners' participation in community-based dog-vaccination programs will be crucial to implementing effective zoonotic disease preventive activities. Spatial and social elements of urbanization play an important role in coverage of MDVC and should be considered during their planning and evaluation

Sampling effort and characteristics of the study population.

Sampling effort and characteristics of the study population.</p

Model selection results for parasite richness among captive primates in Peru.

This table summarizes the generalized linear models (GLM) and generalized linear mixed effects models (GLMM) built to evaluate the contribution of population characteristics to parasite richness. Models ranked by Akaike’s information criterion with small-sample correction (AICc). Statistics include number of parameters (K), log-likelihood (−2LL), difference between AICc of each model and the best model (ΔAICc), and evidence ratio (wi/w1). Models listed under each heading are included in the 95% confidence set. (DOCX)</p

Map of Peru showing the distribution of the study population by context and city.

Pie charts are proportional to the number of monkeys sampled in each city, whether at government-regulated captive facilities (Captivity, black), at households (Pet, light blue), or at markets (Trade, pink). Insert shows the location of Peru in South America. See Table 2 for further details.</p

Factor loadings of the Principal Components (PC) Analysis.

This table shows the correlation of the different parasite genera with the main two principal components explaining the variation between parasite community composition across contexts for animal-human interaction and host genera of trafficked primates in Peru. (DOCX)</p

Prevalence of enteric bacteria in captive monkeys found at each context for animal-human interaction in Peru.

Bar plot showing the proportion of monkeys with positive status for Aeromonas sp., Aeromonas caviae, Aeromonas sobria, Aeromonas hydrophila, Campylobacter sp., Campylobacter jejunii, Campylobacter coli, Plesiomonas shigelloides., Salmonella sp., Shigella boydii, Shigella flexneri, and Shigella sonnei across contexts. (TIF)</p

Parasite community similarities among animal-human contexts.

Principal component (PC) analysis showing the variance in parasite presence among host genera and context in two dimensions. The symbols represent the parasite community of each monkey genus at each animal-human context, and the distance between them illustrates their dissimilarity. Ellipses correspond to the 95% confidence interval for each context.</p