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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., (© 2022 Wiley Periodicals LLC.)

Deeper or more 'severe' linear enamel hypoplasia (LEH) defects are hypothesized to reflect more severe stress during development, but it is not yet clear how depth is influenced by intrinsic enamel growth patterns. Recent work documented inter- and intraspecific differences in LEH defect depth in extant great apes, with mountain gorillas having shallower defects than other taxa, and females having deeper defects than males. Here, we assess the correspondence of inter- and intraspecific defect depth and intrinsic aspects of enamel growth: enamel extension rates, outer enamel striae of Retzius angles, and linear enamel thickness. Thin sections of great ape canines (n = 40) from Gorilla beringei beringei, Gorilla gorilla gorilla, Pan troglodytes, and Pongo spp. were analyzed. Enamel extension rates were calculated within deciles of enamel-dentine junction length. Linear enamel thickness and the angle of intersection between striae of Retzius and the outer enamel surface were measured in the imbricational enamel. Mountain gorillas have faster enamel extension rates and shallower striae angles than the other taxa examined. Mountain gorillas have thinner imbricational enamel than western lowland gorillas and orangutans, but not chimpanzees. In the combined-taxon sample, females exhibit larger striae angles and thicker imbricational enamel than males. Enamel extension rates are highly negatively correlated with striae angles and LEH defect depth. Enamel growth variation corresponds with documented inter- and intraspecific differences in LEH defect depth in great ape canines. Mountain gorillas have shallower striae angles and faster extension rates than other taxa, which might explain their shallow LEH defect morphology and the underestimation of their LEH prevalence in previous studies. These results suggest that stressors of similar magnitude and timing might produce defects of different depths in one species or sex vs. another, which has implications for interpretations of stress histories in hominins with variable enamel growth patterns., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Mountain gorillas ( Gorilla beringei beringei) are one of the most critically endangered great apes in the world. The most common cause of mountain gorilla morbidity and mortality is trauma (e.g., injury from conspecifics or snare entrapment). We conducted a retrospective case-control study of free-ranging, human-habituated mountain gorillas to evaluate factors associated with snare entrapment and the results of clinical intervention. Data were collected from clinical records on all clinical intervention cases ( n=132) in Volcanoes National Park, Rwanda, conducted between 1995-2015. Wildlife veterinarians treated 37 gorillas entrapped in snares and 95 gorillas for other clinical conditions (including trauma and respiratory illness). Multivariate statistical analyses revealed that young gorillas (<8 yr old) were more likely than older gorillas to become snared; that comorbidities delayed times to intervention (≥3 d); and that severity of wounds at the time of intervention were associated with increased risk of lasting impairment (including loss of limb or limb function, or death) within 1 mo after intervention. Our results may influence decisions for gorilla health monitoring and treatment to most effectively conserve this critically endangered species.

Epstein-Barr virus (EBV) infects greater than 90% of humans, is recognized as a significant comorbidity with HIV/AIDS, and is an etiologic agent for some human cancers. The critically endangered mountain gorilla population was suspected of infection with an EBV-like virus based on serology and infant histopathology similar to pulmonary reactive lymphoid hyperplasia (PRLH), a condition associated with EBV in HIV-infected children. To further examine the presence of EBV or an EBV-like virus in mountain gorillas, we conducted the first population-wide survey of oral samples for an EBV-like virus in a nonhuman great ape. We discovered that mountain gorillas are widely infected (n = 143/332) with a specific strain of lymphocryptovirus 1 (GbbLCV-1). Fifty-two percent of infant mountain gorillas were orally shedding GbbLCV-1, suggesting primary infection during this stage of life, similar to what is seen in humans in less developed countries. We then identified GbbLCV-1 in post-mortem infant lung tissues demonstrating histopathological lesions consistent with PRLH, suggesting primary infection with GbbLCV-1 is associated with PRLH in infants. Together, our findings demonstrate that mountain gorilla's infection with GbbLCV-1 could provide valuable information for human disease in a natural great ape setting and have potential conservation implications in this critically endangered species.

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.

In 2007, we detected human herpes simplex virus type 1, which caused stomatitis, in a juvenile confiscated eastern lowland gorilla (Gorilla beringei graueri) that had a high degree of direct contact with human caretakers. Our findings confirm that pathogens can transfer between nonhuman primate hosts and humans.

Mountain gorillas (Gorilla beringei beringei) are critically endangered primates surviving in two isolated populations in protected areas within the Virunga Massif of Rwanda, Uganda, the Democratic Republic of Congo, and in Bwindi Impenetrable National Park in Uganda. Mountain gorillas face intense ecologic pressures due to their proximity to humans. Human communities outside the national parks, and numerous human activities within the national parks (including research, tourism, illegal hunting, and anti-poaching patrols), lead to a high degree of contact between mountain gorillas and wildlife, domestic animals, and humans. To assess the pathogen transmission potential between wildlife and livestock, feces of mountain gorillas, forest buffalo (Syncerus caffer nanus), and domestic cattle (Bos taurus) in Rwanda were examined for the parasites Giardia and Cryptosporidium. Giardia was found in 9% of mountain gorillas, 6% of cattle, and 2% of forest buffalo. Our study represents the first report of Giardia prevalence in forest buffalo. Cryptosporidium-like particles were also observed in all three species. Molecular characterization of Giardia isolates identified zoonotic genotype assemblage B in the gorilla samples and assemblage E in the cattle samples. Significant spatial clustering of Giardia-positive samples was observed in one sector of the park. Although we did not find evidence for transmission of protozoa from forest buffalo to mountain gorillas, the genotypes of Giardia samples isolated from gorillas have been reported in humans, suggesting that the importance of humans in this ecosystem should be more closely evaluated.

Between 1990 and 2010, 18 outbreaks of respiratory disease occurred in Rwanda's wild human-habituated mountain gorillas (Gorilla beringei beringei). An outbreak was defined as clinically observable respiratory illness involving at least one third of all the gorillas in a family group (> 30% morbidity) over the course of at least 7 days. Outbreaks lasted 2 wk to 4 mo and affected up to five different gorilla family groups, either concurrently or sequentially. An outbreak was considered over if no further clinical illness was observed in the same or another group for at least 1 mo. Clinical signs varied from nasal discharge, sneezing, and mild intermittent coughing (mild), to spasmodic coughing, lethargy, and partial anorexia (moderate), to dyspnea, tachypnea, respiratory distress, weakness, complete anorexia, and occasionally death (severe). Nearly every mountain gorilla group habituated for tourism or research in Rwanda experienced at least one outbreak, and they may be increasing in frequency. In the first 15 yr of the review period 1990-2005, there were nine outbreaks involving 16 gorilla groups; in the last 5 yr of the review period, 2006-2010, there were nine outbreaks involving 11 groups. Although most gorillas recovered without treatment, 41 veterinary procedures were required to medically manage 35 severely ill individuals. Given the rise of mountain gorilla ecotourism in Rwanda, the possibility that respiratory disease results from contact with infected humans is of great concern, and both the etiology and epidemiology of this problem are active areas of research. The observed clinical signs, response to antimicrobial therapy among the sickest individuals, and postmortem findings are most consistent with viral upper respiratory tract infections complicated in some cases by secondary bacterial infections. The current gorilla visitation rules have been designed to minimize the risk of disease transmission between humans and wild human-habituated great apes.

The genetic relatedness of mountain gorillas and humans has led to concerns about interspecies transmission of infectious agents. Human-to-gorilla transmission may explain human metapneumovirus in 2 wild mountain gorillas that died during a respiratory disease outbreak in Rwanda in 2009. Surveillance is needed to ensure survival of these critically endangered animals.

Health monitoring of wildlife populations can greatly benefit from rapid, local, noninvasive molecular assays for pathogen detection. Fecal samples collected from free-living Virunga mountain gorillas (Gorilla beringei beringei) between August 2002 and February 2003 were tested for Campylobacter spp. DNA using a portable, real-time polymerase chain reaction (PCR) instrument. A high prevalence of Campylobacter spp. was detected in both individually identified (22/26=85%) and nest-collected samples (68/114=59.6%), with no statistically significant differences among different gorilla sexes or age classes or between tourist-visited versus research gorilla groups. The PCR instrument was able to discriminate two distinct groups of Campylobacter spp. in positive gorilla samples based on the PCR product fluorescent-probe melting profiles. The rare type (6/90 positives, 7%, including three mixed cases) matched DNA sequences of Campylobacter jejuni and was significantly associated with abnormally soft stools. The more common type of positive gorilla samples (87/90 positives, 97%) were normally formed and contained a Campylobacter sp. with DNA matching no published sequences. We speculate that the high prevalence of Campylobacter spp. detected in gorilla fecal samples in this survey mostly reflects previously uncharacterized and nonpathogenic intestinal flora. The real-time PCR assay was more sensitive than bacterial culture with Campylobacter-specific media and commercially available, enzyme immunoassay tests for detecting Campylobacter spp. in human samples.

Cholesterol concentrations in captive gorillas and orangutans vary widely within species and average approximately 244 mg/dl for gorillas and 169 mg/dl for orangutans as published previously. The International Species Inventory System reports higher concentrations of 275 and 199 mg/dl for gorillas and orangutans, respectively. It is unknown whether these values were typical, influenced by captive management, or both. To answer this question, banked serum samples from free-ranging mountain gorillas (Gorilla beringei), western lowland gorillas (Gorilla gorilla gorilla), and Bornean orangutans (Pongo pygmaeus) were analyzed for total cholesterol, triglyceride, high-density lipoprotein cholesterol, and low-density lipoprotein cholesterol concentrations. Mountain gorillas did not differ significantly from free-ranging western lowland gorillas in cholesterol, triglyceride, high-density lipoprotein cholesterol, or low-density lipoprotein cholesterol concentrations, indicating mountain gorilla values could be a model for western lowland gorillas. Captive gorilla total cholesterol and low-density lipoprotein cholesterol concentrations were significantly higher (P < 0.05) than in free-ranging groups. Triglyceride concentrations for captive gorillas were significantly higher (P < 0.05) than the male mountain and western lowland gorillas, but they were not significantly different from the female mountain gorillas. Captive orangutan total cholesterol concentrations were only higher (P < 0.05) than the free-ranging female orangutans, whereas captive orangutan low-density lipoprotein cholesterol concentrations were significantly higher (P < 0.05) than both free-ranging male and female orangutans. Calculated and measured low-density lipoprotein cholesterol concentrations were compared for all free-ranging animals and were significantly different (P < 0.05) for all groups, indicating Friedewald's equation for calculating low-density lipoprotein cholesterol is not appropriate for use with nonfasted apes. The higher total cholesterol and low-density lipoprotein cholesterol concentrations in captive apes may predispose them to cardiovascular disease and might be attributed to diets, limited energy expenditure, and genetics.

Microsporidian spores have been detected by Chromotrope 2R and calcofluor stains in fecal samples of three free-ranging human-habituated mountain gorillas in Uganda and in two people who share gorilla habitats. All spore isolates have been identified by PCR with species-specific primers and fluorescent in situ hybridization with a species-specific oligonucleotide probe to be Encephalitozoon intestinalis. Sequencing analyses of the full length SSUrRNA amplified from all spore isolates were identical with Enc. intestinalis SSUrRNA GenBank SIU09929. Sequences generated from a fragment containing the internal transcribed spacer of these isolates were identical to GenBank sequence Y11611, i.e., Enc. intestinalis of anthroponotic origin. A single pathogen genotype in two genetically distant but geographically united host groups indicates anthropozoonotic transmission of Enc. intestinalis. It is highly unlikely that these two identical Enc. intestinalis genotypes were acquired independently by gorillas and people; it is much more probable that one group initiated infection of the other.

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.