USE OF COMPUTED TOMOGRAPHY (CT) TO DETERMINE THE SENSITIVITY OF CLINICAL SIGNS AS A DIAGNOSTIC TOOL FOR RESPIRATORY DISEASE IN BORNEAN ORANGUTANS (PONGO PYGMAEUS).

Orangutans are noteworthy among great apes in their predilection for chronic, insidious, and ultimately fatal respiratory disease. Termed Orangutan Respiratory Disease Syndrome (ORDS), this cystic fibrosis-like disease is characterized by comorbid conditions of sinusitis, mastoiditis, airsacculitis, bronchiectasis, and recurrent pneumonia. The aim of this retrospective study was to determine the sensitivity of clinical signs in the diagnosis of ORDS in Bornean orangutans (Pongo pygmaeus) compared with the gold standard for diagnosis via computed tomography (CT). We retrospectively compared observed clinical signs with CT imaging in a population of clinically affected animals at an orangutan rescue center in southeastern Borneo. From August 2017 to 2019, this center housed 21 ORDS-affected animals, all of which underwent CT imaging to delineate which areas of the respiratory tract were affected. We reviewed clinical signs recorded in medical records and keeper observation notes for each individual for the period of 2 years prior to the date of the CT scan. A chi-square test of association was used to assess whether the observed clinical signs could predict the results of CT imaging. Results show that clinical signs may not be sensitive indicators in predicting respiratory disease identified by CT imaging. Based on the results of this study, clinical signs appear to be very poor predictors of underlying respiratory pathology in orangutans, based on high P-values, low sensitivity, and low specificity. This result is observed even with clinical signs data gathered over a full 24-mo period prior to CT scan performance. The findings of this study suggest the need for advanced imaging to properly diagnose and manage the most common health issue of captive orangutans.

Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei).

Conservation efforts have led to the recovery of the endangered mountain gorilla populations. Due to their limited potential for spatial expansion, population densities increased, which may alter the epidemiology of infectious diseases. Recently, clinical gastrointestinal illnesses linked to helminth infections have been recorded in both gorilla populations. To understand drivers and patterns of helminth infections we quantified strongylid and tapeworm infections across both Virunga Massif and Bwindi populations using fecal egg counts. We assessed the impact of age, sex, group size, season and spatial differences used as a proxy, which reflects observed variation in the occurrence of gastrointestinal problems, vegetation types, gorilla subpopulation growth and associated social structure on helminth infections. We revealed striking geographic differences in strongylid infections with higher egg counts mostly in areas with high occurrences of gastrointestinal disease. Increased helminth egg counts were also associated with decreasing group size in some areas. Observed spatial differences may reflect mutual effects of variations in subpopulation growth rates, gorilla social structure, and vegetation associated with altitude across mountain gorilla habitat. Helminth infection intensities in Virunga gorillas were lowest in the youngest and the oldest animals. Elucidating parasite infection patterns of endangered species with low genetic diversity is crucial for their conservation management.

USE OF A HUMAN INDIRECT IMMUNOFLUORESCENCE ANTIBODY ASSAY FOR BALAMUTHIA MANDRILLARIS IN A GROUP OF CAPTIVE NORTHWEST BORNEAN ORANGUTANS (PONGO PYGMAEUS PYGMAEUS).

Granulomatous amoebic encephalitis caused by the free-living amoeba Balamuthia mandrillaris is a highly fatal disease that was first isolated from a mandrill (Mandrillus sphinx), and has since been diagnosed in several nonhuman primates including orangutans. Indirect immunofluorescence antibody (IFA) techniques for Balamuthia have been used in the fields of human medicine and epidemiology both for exposure assessment and screening of clinical patients for antemortem diagnosis. Stored serum samples from five captive Northwest Bornean orangutans (Pongo pygmaeus pygmaeus), including one who had died from B. mandrillaris infection, housed at a single facility were screened with a human IFA assay for B. mandrillaris. Only the single, clinically affected individual was seropositive, and the results suggest that the use of the available human B. mandrillaris IFA assay is a novel diagnostic option for detection of Balamuthia antibodies in this species. A validated screening serological test could be used in individuals exhibiting signs consistent with granulomatous amoebic encephalitis to facilitate earlier antemortem diagnosis of Balamuthia infection, which is critical if treatment is to be pursued. This pilot study presents the use of serological detection methods for B. mandrillaris screening in a nonhuman primate. Subsequent use of the B. mandrillaris IFA assay in the larger captive population should be pursued for validation of the test and to provide further information on seroprevalence and evaluation of risk factors for exposure to Balamuthia and subsequent development of disease.

A Sarcina bacterium linked to lethal disease in sanctuary chimpanzees in Sierra Leone.

Human and animal infections with bacteria of the genus Sarcina (family Clostridiaceae) are associated with gastric dilation and emphysematous gastritis. However, the potential roles of sarcinae as commensals or pathogens remain unclear. Here, we investigate a lethal disease of unknown etiology that affects sanctuary chimpanzees (Pan troglodytes verus) in Sierra Leone. The disease, which we have named "epizootic neurologic and gastroenteric syndrome" (ENGS), is characterized by neurologic and gastrointestinal signs and results in death of the animals, even after medical treatment. Using a case-control study design, we show that ENGS is strongly associated with Sarcina infection. The microorganism is distinct from Sarcina ventriculi and other known members of its genus, based on bacterial morphology and growth characteristics. Whole-genome sequencing confirms this distinction and reveals the presence of genetic features that may account for the unusual virulence of the bacterium. Therefore, we propose that this organism be considered the representative of a new species, named "Candidatus Sarcina troglodytae". Our results suggest that a heretofore unrecognized complex of related sarcinae likely exists, some of which may be highly virulent. However, the potential role of "Ca. S. troglodytae" in the etiology of ENGS, alone or in combination with other factors, remains a topic for future research.

Detection of Ebola Virus Antibodies in Fecal Samples of Great Apes in Gabon.

Based on a large study conducted on wild great ape fecal samples collected in regions of Gabon where previous human outbreaks of Ebola virus disease have occurred between 1994 and 2002, we provide evidence for prevalence of Zaire ebolavirus (EBOV)-specific antibodies of 3.9% (immunoglobulin G (IgG)) and 3.5% (immunoglobulin M (IgM)) in chimpanzees and 8.8% (IgG) and 2.4% (IgM) in gorillas. Importantly, we observed a high local prevalence (31.2%) of anti-EBOV IgG antibodies in gorilla samples. This high local rate of positivity among wild great apes raises the question of a spatially and temporally localized increase in EBOV exposure risk and the role that can be played by these animals as sentinels of the virus's spread or reemergence in a given area.

Monitoring great ape heart health through innovative electrocardiogram technology: Training methodologies and welfare implications.

Assessing and treating cardiovascular disease (or heart disease) is a growing concern for institutions housing great apes, as it is a major cause of mortality in all four taxa managed in human care. As part of a proactive monitoring plan, zoological managers and veterinarians often elect to perform electrocardiograms (ECGs) on their great ape populations. ECGs noninvasively evaluate cardiac electrical activity, and are thereby capable of providing information regarding heart function. This electrical signature is transcribed as a visual display of waveforms, referred to as telemetry strips, and can detect irregularities in heart rhythm, also known as arrhythmia. While traditional 6- or 12-lead ECGs are recommended periodically as part of a thorough heart performance evaluation, here we discuss the KardiaMobile (KM) device as an additional primate welfare tool. KM is a small, Food and Drug Administration-cleared, clinical-grade mobile ECG monitor that requires only 30 s of pressure to flag heart rate or arrhythmic abnormalities. We detail the training process and applicability to great apes in human care.

Hyperglycemic hyperosmolar state in a chimpanzee (Pan troglodytes).

A 19-year-old female chimpanzee (Pan troglodytes) presented for cachexia, acute weakness, hyporexia, icterus, and polyuria. The animal was diagnosed with a hyperglycemic hyperosmolar state, which is a well-recognized syndrome in diabetic humans that is rarely diagnosed in animals. This case documents an important and likely under-reported syndrome in non-human primates.

Brunner's gland hyperplasia in a geriatric chimpanzee (Pan troglodytes), an infrequently reported lesion.

Benign duodenal tumours have very rarely been reported in captive non-human primates and are also rare in human beings. Brunner's gland hyperplasia has not been fully described in a non-human primate. Here, we report Brunner's gland hyperplasia in a geriatric chimpanzee, which was an incidental finding during post-mortem examination.

Evaluating Ketosis in Primate Field Studies: Validation of Urine Test Strips in Wild Bornean Orangutans (Pongo pygmaeus wurmbii).

The use of urine test strips (e.g., Roche Chemstrip®) has become the standard for quickly assessing the physiological condition and/or health of wild primates. These strips have been used to detect ketosis as a marker of fat catabolism in several primate taxa in their natural environments in response to changing food availability. However, the use of urine strips to determine ketosis has only been validated in human studies, and thus it remains unclear whether these strips accurately detect and quantify ketone bodies in nonhuman primates. We examined variations in ketone body concentrations in urine samples collected from wild Bornean orangutans at the Tuanan Orangutan Research Station. We assessed the accuracy of qualitative results from Chemstrip test strips in the field (i.e., negative, small, moderate, and large) using an enzyme-linked assay in the laboratory to determine the concentrations of acetoacetate of the same urine samples. Urine samples that tested positive for ketones in the field had significantly higher levels of ketones in the enzymatic assay compared to those that tested negative. There was significant variation in acetoacetate concentrations among the 4 Chemstrip values; however, post hoc tests revealed no significant differences between negative and small samples. We conclude that urinary test strips provide a useful tool for determining ketotic state in wild orangutans, but caution should be taken when interpreting results from samples showing only small levels of ketones on these strips.

DIFFUSE IDIOPATHIC SKELETAL HYPEROSTOSIS IN CAPTIVE GORILLAS (GORILLA SPP.): APPEARANCES AND DIAGNOSIS.

Diffuse idiopathic skeletal hyperostosis (DISH) is a disorder of unknown cause, in which new bone forms in soft tissues attached to the skeleton. Originally described in humans, in whom it is quite common, it is usually asymptomatic. New bone may completely bridge across joints, especially in the spine. However, it can be difficult to distinguish from diseases such as spondyloarthritis and spondylosis. With safer and increased use of radiography in diagnosis, the unfamiliar skeletal changes of asymptomatic DISH may now be coincidentally revealed during investigation of other disorders and result in misdiagnosis and unnecessary treatment. There have been case reports of its occurrence in great apes, but this is the first study to illustrate its appearances in a series of 11 skeletons of western and eastern lowland gorillas (Gorilla gorilla gorilla and Gorilla beringei graueri) from zoos in Europe and the United States. The study combines a review of available clinical and postmortem records with examination of the skeletons and radiologic investigation, such as computed tomography (CT). The results indicate that the disorder is probably common in older (>30 yr) captive gorillas, but that it is asymptomatic. It was not symptomatic during life in any of these animals. Several cases had unexpected features, such as extensive involvement of the thorax and extra-articular sacroiliac and tibiofibular joint fusions that are not typical in humans. By illustrating these skeletons, the study should aid differentiation of DISH from spondylosis (syn spondylosis deformans) and spondyloarhritis. It illustrates those features that are atypical of human DISH. CT scanning is valuable in such cases for examining diagnostically important areas such as sacroiliac joints. Increased awareness of DISH should help with understanding its cause, both in gorillas and humans.

ALVEOLAR ECHINOCOCCOSIS IN WESTERN LOWLAND GORILLAS (GORILLA GORILLA GORILLA): ALBENDAZOLE WAS NOT ABLE TO STOP PROGRESSION OF THE DISEASE.

Echinococcus multilocularis is the etiologic agent of alveolar echinococcosis (AE), a severe and potentially fatal larval cestode infection primarily affecting the liver. AE is known to occur in dead-end intermediate hosts, including humans and nonhuman primates. Between 1999 and 2016, AE was diagnosed in seven western lowland gorillas (Gorilla gorilla gorilla), all from a Swiss zoo. Six gorillas died of the disease. One individual is still alive, receives continuous albendazole medication, and shows no clinical signs. Most infected animals remained asymptomatic for years. Only one young gorilla showed early signs of acute discomfort and abdominal pain. In the final stage of the disease, affected animals died suddenly, or showed a short course of nonspecific but severe clinical signs, including lethargy, recumbency, abdominal enlargement, and anorexia. Postmortem examination confirmed hepatic AE complicated by peritonitis in most cases. Echinococcus multilocularis infection may remain undetected because of a very long incubation period. Hematological and biochemical parameters rarely showed abnormalities in this phase. Thus, inclusion of abdominal hepatic ultrasound examination and serology is recommended for early AE detection in routine examinations of gorillas in endemic areas or where food is potentially contaminated with E. multilocularis eggs. Ultrasound or computed tomography was useful to monitor progression and to estimate the volumetric extension of the hepatic lesions. Current medication with albendazole, which proved to be effective for human patients, was not able to stop progression of hepatic lesions in gorillas. Therefore, its therapeutic value remains questionable in gorillas. However, long-term oral albendazole treatment proved to be safe, and therapeutic plasma levels published for humans were achieved. Preventive measures such as thermo-treatment of food or vaccination of gorillas and other nonhuman primates should be considered in areas where E. multilocularis is present.

Diagnosing cardiovascular disease in western lowland gorillas (Gorilla gorilla gorilla) with brain natriuretic peptide.

Cardiovascular disease is a leading cause of death in zoo-housed great apes, accounting for 41% of adult gorilla death in North American zoological institutions. Obtaining a timely and accurate diagnosis of cardiovascular disease in gorillas is challenging, relying on echocardiography which generally requires anesthetic medications that may confound findings and can cause severe side effects in cardiovascularly compromised animals. The measurement of brain natriuretic peptide (BNP) has emerged as a modality of interest in the diagnosis, prognosis and treatment of human patients with heart failure. This study evaluated records for 116 zoo-housed gorillas to determine relationships of BNP with cardiovascular disease. Elevations of BNP levels correlated with the presence of visible echocardiographic abnormalities, as well as reported clinical signs in affected gorillas. Levels of BNP greater 150 pb/mL should alert the clinician to the presence of myocardial strain and volume overload, warranting medical evaluation and intervention.

Lipoid pneumonia in an orangutan (Pongo abelii) with chronic respiratory problems.

An orangutan (Pongo abelii) presented with chronic respiratory problems. Cytological evaluation of the bronchoalveolar lavage fluids revealed macrophages with well-circumscribed intracytoplasmic clear vacuoles and lipid droplets in the background, confirmed by Oil Red O staining. The findings were indicative of lipoid pneumonia. This is the first report of lipoid pneumonia in an orangutan.

Tinea corporis by Microsporum audouinii in a female chimpanzee (Pan troglodytes) from Guinea-Bissau: A case report.

We report a Microsporum audouinii infection in a female juvenile chimpanzee (Pan troglodytes) presenting generalized dermatitis compatible with dermatophytosis. Dermatophyte was identified by macro- and microscopic characterization of skin and scales cultures in Mycosel Agar. The topical treatment applied was effective, having the potential for dermatophytosis treatment in immunocompetent primates.

REVIEW: PSYCHOPATHOLOGIES IN CAPTIVE NONHUMAN PRIMATES AND APPROACHES TO DIAGNOSIS AND TREATMENT.

Despite the growing knowledge and literature on primate medicine, assessment and treatment of behavioral abnormalities in nonhuman primates (NHPs) is an underdeveloped field. There is ample evidence for similarity between humans and great apes, including basic neurologic physiology and emotional processes, and no substantial argument exists against a concept of continuity for abnormal conditions in NHPs that emerge in response to adverse experiences, akin to human psychopathology. NHPs have served as models for human psychopathologies for many decades, but the acquired knowledge has only hesitantly been applied to primates themselves. This review aims to raise awareness among the veterinary community of the wealth of literature on NHP psychopathologies in human medicine and anthropology literature and calls for the necessity to include mental health assessments and professionally structured treatment approaches in NHP medicine. Growing understanding about causes and pathogenesis of abnormal behavior in NHP will not only help to prevent the development of undesirable behaviors but also allow for treatment and management of long-lived, already affected animal patients.

Visceral leishmaniasis in an infant gorilla (Gorilla gorilla gorilla): Clinical signs, diagnosis, and successful treatment with single-dose liposomal amphotericin B.

A 2-year-old captive gorilla (Gorilla gorilla gorilla) was diagnosed with visceral leishmaniasis in Brazil, and treated with a single dose of liposomal amphotericin B, which resulted in clinical cure. This is the first report of visceral leishmaniasis in gorillas, and the first reported liposomal amphotericin B treatment in great apes.

Treatment of disseminated Strongyloides spp. infection in an infant Sumatran orangutan (Pongo abelii).

Strongyloides nematodes have been reported in all species of great apes with orangutans ≤5 years old most susceptible to severe clinical disease. This brief communication describes the first published case of antemortem diagnosis and treatment of disseminated strongyloidiasis in a clinically affected 5-month-old Sumatran orangutan (Pongo abelii).

Amelogenesis imperfecta in the dentition of a wild chimpanzee.

This report describes a case of amelogenesis imperfecta in the dentition of a female chimpanzee. Amelogenesis imperfecta is a group of rare genetic conditions that create severe enamel defects, which, although well researched in humans, has not yet been investigated in wild non-human primates.

Case study: Scoliosis in a Bonobo (Pan paniscus).

Differential diagnosis of observed morphological features on an adult male bonobo skeleton was consistent with idiopathic scoliosis. Directional asymmetry was an order of magnitude higher compared with asymptomatic skeletons. This possible case of idiopathic scoliosis contributes to data that suggest a weaker tie between bipedalism and scoliosis than previously hypothesized.

Vernal-like conjunctivitis in a western lowland gorilla (Gorilla gorilla gorilla).

CASE DESCRIPTION: A 17-year-old female western lowland gorilla presented with bilateral ocular discharge, conjunctivitis, and rhinitis that was investigated and treated over a 34-month period. Clinical findings, diagnostic results, treatment, and follow-up are described. CLINICAL FINDING: A mild intermittent mucoid ocular discharge was initially noted. 10 months later, conjunctival hyperemia and thickening developed and progressed rapidly to a mass-like lesion covering the right eye. Hematology revealed eosinophilia. Conjunctival cytology revealed eosinophils and neutrophils, and histopathology revealed a chronic proliferative eosinophilic conjunctivitis. 21 months after, the ocular lesions were investigated the gorilla developed masses within both external nares. Histopathology of the nasal lesions revealed chronic-active eosinophilic rhinitis. TREATMENT AND OUTCOME: Treatment of the gorilla was based on protocols recommended for human patients. Protocols for mild, moderate, and finally severe disease were used, involving topical and oral combinations of treatments. The gorilla eventually responded to systemic immunosuppressant therapy recommended for severe refractory disease. CLINICAL SIGNIFICANCE: To the authors' knowledge, this is the first reported case of vernal-like conjunctivitis in a western lowland gorilla.