Opportunities for respiratory disease transmission from people to chimpanzees at an East African tourism site.

Respiratory illnesses, including COVID-19, present a serious threat to endangered wild chimpanzee (Pan troglodytes) populations. In some parts of sub-Saharan Africa, chimpanzee tracking is a popular tourism activity, offering visitors a chance to view apes in their natural habitats. Chimpanzee tourism is an important source of revenue and thus benefits conservation; however, chimpanzee tracking may also increase the risk of disease transmission from people to chimpanzees directly (e.g., via aerosol transmission) or indirectly (e.g., through the environment or via fomites). This study assessed how tourist behaviors might facilitate respiratory disease transmission at a chimpanzee tracking site in Kibale National Park, Uganda. We observed tourists, guides, and student interns from the time they entered the forest to view the chimpanzees until they left the forest and noted behaviors related to disease transmission. Common behaviors included coughing, sneezing, and urinating, which respectively occurred during 88.1%, 65.4%, and 36.6% of excursions. Per excursion, individuals touched their faces an average of 125.84 ± 34.45 times and touched large tree trunks or branches (which chimpanzees might subsequently touch) an average of 230.14 ± 108.66 times. These results show that many pathways exist by which pathogens might move from humans to chimpanzees in the context of tourism. Guidelines for minimizing the risk of such transmission should consider tourist behavior and the full range of modes by which pathogen transmission might occur between tourists and chimpanzees.

The character of parietal and orbital alterations in the superfamily Hominoidea (families Hominidae [exclusive of Homo] and Hylobotidae).

Parietal external surface disruption routinely referred to as porotic hyperostosis, and orbital alterations (cribra orbitalia), have been attributed to anemia-related bone marrow hyperplasia in humans. A recent study in humans identified that they were actually vascular in nature. Skeletons were examined and epi-illumination surface microscopy was performed on the parietal region and orbit of 156 Hominidae and 123 Hylobotidae to assess if these phenomena were trans-phylogenetic. Trans-cortical channels were recognized on the basis of visualized ectocranial surface defects penetrating the parietal; cribra orbitalia, by alteration of the normally smooth orbital roof appearance. Trans-cortical parietal channels, ranging in size from 20 to 100 µm, are rare in Gorilla and Pan troglodytes and absent in Pan paniscus. They are universally present in adult Pongo abeli and in Hylobatidae, independent of species. Cribra orbitalia was common in Hylobotidae, Pongo pygmaeus and P. abelii, less prevalent in adult P. troglodytes, and not recognized in any Gorilla gorilla or P. paniscus examined. The proliferative form predominated, with the exception of Hylobates concolor and muelleri, in which uncalcified vascular grooves predominated. No correlation was observed between the presence of either trans-cortical channels or cribra orbitalia and fractures, osteoarthritis, or inflammatory arthritis. Parietal alterations observed in apes are trans-cortical channels, analogous to those observed in humans, and do not represent porosity. Similarly, cribra orbitalia in apes is confirmed as vascular in nature. The proliferative form apparently represents calcification of blood vessel walls, indistinguishable from observations in humans. Predominant presence in adults rather than in juveniles suggests that both forms are acquired rather than developmental in derivation. Sex and bone alteration/disease-independence suggests that mechanical, endocrine, and inflammatory phenomena do not contribute to the development of either. Further, independent occurrence of trans-cortical channels and cribra orbitalia suggests that they do not have a shared etiology.

Cardiac disease is linked to adiposity in male gorillas (Gorilla gorilla gorilla).

Cardiac disease is a major cause of morbidity and mortality for adult gorillas. Previous research indicates a sex-based difference with predominantly males demonstrating evidence of left ventricular hypertrophy. To evaluate these findings, we analyzed serum markers with cardiac measures in a large sample of gorillas. The study sample included 44 male and 25 female gorillas housed at American Association of Zoo and Aquariums (AZA)-accredited zoos. Serum samples were collected from fasted gorillas during routine veterinary health exams and analyzed to measure leptin, adiponectin, IGF-1, insulin, ferritin, glucose, triglycerides, and cholesterol. Cardiac ultrasonography via transthoracic echocardiogram was performed simultaneously. Three echocardiographic parameters were chosen to assess cardiac disease according to parameters established for captive lowland gorillas: left ventricular internal diameter, inter-ventricular septum thickness, and left ventricular posterior wall thickness. Our data revealed that high leptin, low adiponectin, and lowered cholesterol were significantly and positively correlated with measures of heart thickness and age in males but not in females. Lowered cholesterol in this population would be categorized as elevated in humans. High leptin and low adiponectin are indicative of increased adiposity and suggests a potential parallel with human obesity and cardiovascular disease in males. Interestingly, while females exhibited increased adiposity with age, they did not progress to cardiac disease.

Standard growth and diarrhea-associated growth faltering in captive infant rhesus macaques (Macaca mulatta).

Reference growth studies of captive rhesus macaque infants have not accounted for diarrhea and the potential for growth stunting or growth faltering. Healthy infants without diarrhea could be used to build a standard growth chart and a tool used to detect growth faltering associated with diarrhea. We hypothesized infants who develop diarrhea during the first year of life would experience decreased linear weight gain compared to healthy infants, and we used healthy infants to establish standard growth of male and female infants. We hypothesized the lower 3rd percentile of standard growth would be cut-off criteria used in screening for diarrhea-associated growth faltering. Using a retrospective cohort of 6,510 infant weight records in a multiple linear regression, daily weight gain through the first year of life was determined by sex, housing type, and health status. Male standard growth was 4.1 g/day (95%CI: 4.0-4.2 g/day) in corrals and 4.7 g/day (95%CI: 4.5-4.8 g/day) in shelter housing. Female standard growth was 4.0 g/day (95%CI: 3.8-4.2 g/day) in corrals and 4.4 g/day (95%CI: 4.0-4.7 g/day) in shelter housing. Diarrhea was significantly associated with decreased linear weight gain by up to 34% during the first year of life. Odds of growth faltering of infants, defined as those falling below the 3rd percentile of standard growth, were at least 8.9 higher given a history of diarrhea compared to healthy. The growth faltering cut-off criteria had a sensitivity of at least 53% for males and females to screen for diarrhea in infants between 6 and 12 months in shelters housing. Interinstitutional collaborations of infant rhesus macaque weight records would refine the standard growth charts and cut-off criteria, and additional morphometric data would provide a more nuanced picture of growth stunting.

Behavioral studies and veterinary management of orangutans at Bukit Merah Orang Utan Island, Perak, Malaysia.

The Bukit Merah Orang Utan Island (OUI) Foundation has been conducting behavioral and veterinary research on orangutans as an attempt at ex situ conservation. Since 2010, the Primate Research Institute, Kyoto University has been collaborating with OUI to promote environmental enrichment and infant rearing by biological mothers in addition to the continuous efforts of refining the veterinary management of the endangered species. In 2011, three Bornean orangutans (Pongo pygmaeus pygmaeus) were released on an island, called BJ Island, adjacent to OUI. This island is approximately 5.6 ha in size, and 635 trees belonging to 102 plant species were identified prior to their release. Behavioral monitoring of the released individuals has been conducted to evaluate their behavioral adaptation to the new environment. Two of the three released orangutans were born in the wild, whereas the youngest individual was born on OUI and expected to learn forest survival strategies from the two older individuals. One of the orangutans was pregnant at the time of release and subsequently gave birth to two male infants on BJ Island. The behavioral monitoring indicated that these orangutans traveled more and spent more time on trees following their release onto BJ Island. However, resting was longer for two females both on OUI and BJ Island when compared to other populations. The orangutans consumed some natural food resources on BJ Island. The release into a more naturalistic environment may help the orangutans to develop more naturalistic behavioral patterns that resemble their wild counterparts.

Apnea induction for invasive lung function testing in infant olive baboons: Comparison of intravenous propofol versus hyperventilation.

BACKGROUND: In various types of pulmonary research, pulmonary function testing (PFT) is performed to quantify the severity of lung disease. Induction of apnea and positive pressure ventilation are required for accurate PFT measurements in non-cooperative subjects. We compared two methods of apnea induction in infant olive baboons (Papio anubis). METHODS: Pulmonary function testing results were compared during apnea induced by hyperventilation (CO2 washout) vs. intravenous propofol (1 dose 10 mg/kg). PFT was evaluated using a hot-wire pneumotachometer incorporated within an Avea ventilator in nine 1-month-old baboons. RESULTS: Propofol induced apnea faster and more reliably. In both groups, PFT values passed the statistical equivalence test and were not significantly different (Student's t-test). There was a trend toward less data variability after propofol administration. CONCLUSIONS: Intravenous propofol was non-inferior to CO2 washout for apnea induction in infant olive baboons. Propofol induced apnea faster and more reliably and yielded less variable PFT results.

Natural pathology of the captive chimpanzee (Pan troglodytes): A 35-year review.

We present the spontaneous pathological lesions identified as a result of necropsy or biopsy for 245 chimpanzees (Pan troglodytes) over a 35-year period. A review of the pathology database was performed for all diagnoses on chimpanzees from 1980 to 2014. All morphologic diagnoses, associated system, organ, etiology, and demographic information were reviewed and analyzed. Cardiomyopathy was the most frequent lesion observed followed by hemosiderosis, hyperplasia, nematodiasis, edema, and hemorrhage. The most frequently affected systems were the gastrointestinal, cardiovascular, urogenital, respiratory, and lymphatic/hematopoietic systems. The most common etiology was undetermined, followed by degenerative, physiologic, neoplastic, parasitic, and bacterial. Perinatal and infant animals were mostly affected by physiologic etiologies and chimpanzee-induced trauma. Bacterial and physiologic etiologies were more common in juvenile animals. Degenerative and physiologic (and neoplastic in geriatric animals) etiologies predominated in adult, middle aged, and geriatric chimpanzees.

Successful treatment of infertility in a female Sumatran orangutan Pongo abelii.

In 2011, a female Sumatran orangutan housed at Durrell Wildlife Conservation Trust became infertile following a massive antepartum hemorrhage in labor and the delivery of a stillborn infant. The placenta was infected with Pantoea sp. Hysterosalpingography (HSG) revealed blocked fallopian tubes, and pressurized fallopian tube perfusion was used to reverse the tubal occlusion. She subsequently conceived and following an intensive training program, we were able to measure umbilical artery waveform analysis for fetal well-being and placental localization to exclude placenta previa, which could complicate pregnancy and lead to catastrophic hemorrhage. The female went on to deliver a healthy offspring. We suggest that these techniques should be considered for other infertile females in the global captive population.

Natural mortality and cause of death analysis of the captive chimpanzee (Pan troglodytes): A 35-year review.

We present the spontaneous causes of mortality for 137 chimpanzees (Pan troglodytes) over a 35-year period. A record review of the pathology database was performed and a primary cause of mortality was determined for each chimpanzee. The most common causes of mortality were as follows: cardiomyopathy (40% of all mortalities), stillbirth/abortion, acute myocardial necrosis, chimpanzee-induced trauma, amyloidosis, and pneumonia. Five morphologic diagnoses accounted for 61% of mortalities: cardiomyopathy, hemorrhage, acute myocardial necrosis, amyloidosis, and pneumonia. The most common etiologies were degenerative, undetermined, bacterial, traumatic, and neoplastic. The cardiovascular system was most frequently involved, followed by the gastrointestinal, respiratory, and multisystemic diseases. Degenerative diseases were the primary etiological cause of mortality of the adult captive chimpanzee population. Chimpanzee-induced trauma was the major etiological cause of mortality among the perinatal and infant population. This information should be a useful resource for veterinarians and researchers working with chimpanzees.

Long-sightedness in old wild bonobos during grooming.

Some scientists have suggested that, among Hominidae, prolonged postmenopausal longevity evolved uniquely in humans [1], while others disagree [2]. There have, however, been few empirical studies on how physiological aging and somatic durability in humans compare to our closest relatives - chimpanzees and bonobos [3]. If prolonged lifespan is selected for in humans, physiological aging, including reproductive and somatic senescence, might be different for Pan and Homo. But it seems that the parameters of reproductive senescence, such as the age of having their final offspring and the number of years between generations, are not very different between chimpanzee and human females [4]. Here, we report evidence for five cases of long-sightedness (presbyopia) in old wild bonobos, exhibited during grooming. Our results suggest that senescence of the eye has not changed much since the divergence of Pan and Homo from their common ancestor.

Spatial and Temporal Dynamics of a Mortality Event among Central African Great Apes.

In 2006-2007 we observed an unusual mortality event among apes in northern Republic of Congo that, although not diagnostically confirmed, we believe to have been a disease outbreak. In 2007-2011 we conducted ape nest surveys in the region, recording 11,835 G. g. gorilla nests (2,262 groups) and 5,548 P. t. troglodytes nests (2,139 groups). We developed a statistical model to determine likely points of origin of the outbreak to help identify variables associated with disease emergence and spread. We modeled disease spread across the study area, using suitable habitat conditions for apes as proxy for local ape densities. Infectious status outputs from that spread model were then used alongside vegetation, temperature, precipitation and human impact factors as explanatory variables in a Generalized Linear Model framework to explain observed 2007-2011 ape nest trends in the region. The best models predicted emergence in the western region of Odzala-Kokoua National Park and north of the last confirmed Ebola virus disease epizootics. Roads were consistently associated with attenuation of modeled virus spread. As disease is amongst the leading threats to great apes, gaining a better understanding of disease transmission dynamics in these species is imperative. Identifying ecological drivers underpinning a disease emergence event and transmission dynamics in apes is critical to creating better predictive models to guide wildlife management, develop potential protective measures for wildlife and to reduce potential zoonotic transmission to humans. The results of our model represent an important step in understanding variables related to great ape disease ecology in Central Africa.

On the apparent rarity of epithelial cancers in captive chimpanzees.

Malignant neoplasms arising from epithelial cells are called carcinomas. Such cancers are diagnosed in about one in three humans in 'developed' countries, with the most common sites affected being lung, breast, prostate, colon, ovary and pancreas. By contrast, carcinomas are said to be rare in captive chimpanzees, which share more than 99% protein sequence homology with humans (and possibly in other related 'great apes'-bonobos, gorillas and orangutans). Simple ascertainment bias is an unlikely explanation, as these nonhuman hominids are recipients of excellent veterinary care in research facilities and zoos, and are typically subjected to necropsies when they die. In keeping with this notion, benign tumours and cancers that are less common in humans are well documented in this population. In this brief overview, we discuss other possible explanations for the reported rarity of carcinomas in our closest evolutionary cousins, including inadequacy of numbers surveyed, differences in life expectancy, diet, genetic susceptibility, immune responses or their microbiomes, and other potential environmental factors. We conclude that while relative carcinoma risk is a likely difference between humans and chimpanzees (and possibly other 'great apes'), a more systematic survey of available data is required for validation of this claim.

Craniocerebral gunshot wound in a baby chimpanzee--an uncommon experience of neurosurgical treatment conducted in the Guinean forest.

An orphan female chimpanzee was wounded by a left craniocerebral gunshot complicated with a right hemiparesis. Local treatment and long-term antibiotherapy failed to lead to healing. A neurosurgical procedure was planned and achieved. She fully recovered, and 2 years after the procedure, there is no evidence of infection.

Post-injection sciatic neuropathy in a cynomolgus macaque (Macaca fascicularis).

BACKGROUND: Intramuscular injection is a common route parenteral used in primates. METHODS: A cynomolgus macaque was evaluated for acute lameness and atrophy of the left leg with no evidence of trauma. RESULTS: History revealed ketamine injection 12 days prior. CONCLUSIONS: Histologic examination supported traumatic injection neuropathy due to intramuscular injection.

Field immobilization for treatment of an unknown illness in a wild chimpanzee (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania: findings, challenges, and lessons learned.

Infectious diseases are widely presumed to be one of the greatest threats to ape conservation in the wild. Human diseases are of particular concern, and the costs and benefits of human presence in protected areas with apes are regularly debated. While numerous syndromes with fatal outcomes have recently been described, precise identification of pathogens remains difficult. These diagnostic difficulties are compounded by the fact that direct veterinary intervention on wild apes is quite rare. Here we present the unique case of a wild chimpanzee at Gombe National Park that was observed with a severe illness and was subsequently examined and treated in the field. Multiple specimens were collected and tested with the aim of identifying the pathogen responsible for the illness. Our findings represent the first extensive screening of a living wild chimpanzee, yet despite our efforts, the cause and source of illness remain unknown. Nevertheless, our findings represent valuable baseline data for the ape conservation community and for comparison with other recent findings. In addition, we present the case here to demonstrate the planning required and multiple types of expertise necessary to maximize the amount of data obtained from such a rare intervention, and to provide lessons learned for future studies.

Observational monitoring of clinical signs during the last stage of habituation in a wild western gorilla group at Bai Hokou, Central African Republic.

Anthropozoonotic disease transmission to great apes is a critical conservation concern, and has raised ethical doubts regarding ape habituation. We monitored over a 3-year period clinical signs within a group of wild western gorillas (G. gorilla) undergoing habituation at Bai Hokou, Central African Republic. The majority of observations consisted of singular coughs and sneezes among the gorillas. These were the only clinical signs that significantly and positively increased over the years. No changes in the demography of the study group were observed. While clinical signs are not necessarily indicative of 'disease' or other health-related problems, we discuss how long-term records of clinical signs provide useful information when health monitoring, and the importance of the rigid application of preventive disease transmission protocols.

Behavioral recovery from tetraparesis in a captive chimpanzee.

An adult male chimpanzee living in a captive social group at the Primate Research Institute of Kyoto University developed acute tetraparesis. He was paralyzed and received intensive care and veterinary treatment as previously reported in Miyabe-Nishiwaki et al. (J Med Primatol 39:336-346, 2010). The behavioral recovery of the chimpanzee was longitudinally monitored using an index of upright posture between 0 and 41 months after the onset of tetraparesis. Four phases were identified during the course of behavioral recovery. During Phase 0 (0-13 months), the chimpanzee remained lying on his back during the absence of human caretakers. An increase in upright posture occurred in Phase I (14-17 months), then remained at a stable level of around 50-70 % in Phase II (18-29 months). During Phases I and II, the subject's small treatment cage represented a spatial limitation. Thus, behavioral recovery was mainly mediated by arm muscle strengthening caused by raising the body trunk with the aid of materials attached to the cage walls as environmental enrichment. When the chimpanzee was moved to a larger rehabilitation room in Phase III (30-41 months), the percentage of upright posture constantly exceeded 80 %, except in the 40th month when he injured his ankle and was inactive for several days. The enlargement of the living space had a positive effect on behavioral recovery by increasing the types of locomotion exhibited by the subject, including the use of legs during walking. Rehabilitation works were applied in face-to-face situations which enabled the use of rehabilitation methods used in humans. The process of behavioral recovery reported in this study provides a basic data set for planning future rehabilitation programs and for comparisons with further cases of physical disability in non-human primates.

Scheuermann kyphosis in nonhuman primates.

STUDY DESIGN: A cadaveric survey of the thoracic spines of extant species of nonbipedal primates for the presence of Scheuermann kyphosis. OBJECTIVE: To determine the presence and prevalence of Scheuermann kyphosis in quadrupedal species of the closest living relatives to humans to demonstrate that bipedalism is not an absolute requirement for the development of Scheuermann kyphosis. SUMMARY OF BACKGROUND DATA: The etiology of Scheuermann kyphosis remains poorly understood. Biomechanical factors associated with upright posture are thought to play a role in the development of the disorder. To date, Scheuermann kyphosis has been described only in humans and extinct species of bipedal hominids. METHODS: Thoracic vertebrae from 92 specimens of Pan troglodytes (chimpanzee) and 105 specimens of Gorilla gorilla (gorilla) from the Hamann-Todd Osteological Collection at the Cleveland Museum of Natural History were examined for Scheuermann kyphosis on the basis of Sorenson criteria and the presence of anterior vertebral body extensions and for the presence of Schmorl nodes. RESULTS: Two specimens of P. troglodytes (2.2%) were found to have anatomic features consistent with Scheuermann kyphosis including vertebral body wedging greater than 5° at 3 or more adjacent levels and the presence of anterior vertebral body extensions. One of the affected specimens (50%) demonstrated the presence of Schmorl nodes whereas 2 of the unaffected specimens (2.2%) had Schmorl nodes. None of the specimens of G. gorilla (0%) were found to have anterior vertebral body extensions characteristic of Scheuermann kyphosis or Schmorl nodes. CONCLUSION: Thoracic kyphotic deformity consistent with Scheuermann kyphosis exists in quadrupedal nonhuman primates. Bipedalism is not a strict requirement for the development of Scheuermann kyphosis, and the evolutionary origins of the disease predate the vertebral adaptations of bipedal locomotion.

Upper respiratory tract disease in captive orangutans (Pongo sp.): prevalence in 20 European zoos and predisposing factors.

BACKGROUND: Upper respiratory tract disease (URTD) is a significant cause of morbidity in captive orangutans (Pongo abelii, Pongo pygmaeus), and the pathogenesis is often unknown. METHODS: The prevalence of respiratory disease in captive European orangutans (201 animals; 20 zoos) and possible predisposing factors were investigated. RESULTS: Bornean orangutans (P. pygmaeus) showed chronic respiratory signs significantly more often (13.8%) than Sumatran (P. abelii; 3.6%), and males (15.8%) were more often afflicted than females (3.9%). Hand-reared animals (21%) developed air sacculitis more often than parent-reared animals (5%). Diseased animals were more often genetically related to animals with respiratory diseases (93%) than to healthy animals (54%). None of the environmental conditions investigated had a significant effect on disease prevalence. CONCLUSION: Results suggest a higher importance of individual factors for the development of URTD than environmental conditions. Bornean, male and hand-reared orangutans and animals related to diseased animals need increased medical surveillance for early detection of respiratory disease.