Body mass and growth rates in captive chimpanzees (Pan troglodytes) cared for in African wildlife sanctuaries, zoological institutions, and research facilities.

Captive chimpanzees (Pan troglodytes) mature earlier in body mass and have a greater growth rate compared to wild individuals. However, relatively little is known about how growth parameters compare between chimpanzees living in different captive environments. To investigate, body mass was measured in 298 African sanctuary chimpanzees and was acquired from 1030 zoological and 442 research chimpanzees, using data repositories. An analysis of covariance, adjusting for age, was performed to assess same-sex body mass differences between adult sanctuary, zoological, and research populations. Piecewise linear regression was performed to estimate sex-specific growth rates and the age at maturation, which were compared between sexes and across populations using extra-sum-of-squares F tests. Adult body mass was greater in the zoological and resarch populations compared to the sanctuary chimpanzees, in both sexes. Male and female sanctuary chimpanzees were estimated to have a slower rate of growth compared with their zoological and research counterparts. Additionally, male sanctuary chimpanzees were estimated to have an older age at maturation for body mass compared with zoological and research males, whereas the age at maturation was similar across female populations. For both the zoological and research populations, the estimated growth rate was greater in males compared to females. Together, these data contribute to current understanding of growth and maturation in this species and suggest marked differences between the growth patterns of chimpanzees living in different captive environments.

Vitamin D status in chimpanzees in human care: a Europe wide study.

While vitamin D deficiency is a public health concern in humans, comparatively little is known about vitamin D levels in non-human primates. Vitamin D plays a crucial role in overall health and its deficiency is associated with a range of disorders, including cardiovascular disease, which is a leading cause of death in great apes. Serum samples (n = 245) from chimpanzees (Pan troglodytes) housed at 32 European zoos were measured for 25-hydroxyvitamin D2, 25-hydroxyvitamin D3 and total 25-hydroxyvitamin D (25-OHD) using liquid chromatography and tandem mass spectrometry. Of these samples, 33.1% indicated inadequate vitamin D status, using the human reference interval (25-OHD < 50 nmol/L). The season of the year, health status of the animal, and the provision of daily outdoor access had a significant effect on vitamin D status. This is the first large-scale study on vitamin D status of non-human great apes in human care. Inadequate 25-OHD serum concentrations are widespread in the chimpanzee population in Europe and could be a risk factor for the development of idiopathic myocardial fibrosis, a major cause of mortality in this species, as well as other diseases. A review of husbandry and nutrition practices is recommended to ensure optimal vitamin D supply for these endangered animals.

Periodontal health, neutrophil activity and cardiovascular health in captive chimpanzees.

OBJECTIVE: To investigate the association of dental and cardiac disease in a cohort of captive chimpanzees DESIGN: 12 captive chimpanzees underwent periodontal and cardiac examinations under anaesthesia during a relocation to a new enclosure. Blood samples were taken for analysis of circulating markers of cardiac health, nutritional status and isolation of neutrophils for functional assays. They were then observed for three years for signs of heart disease. RESULTS: Although the chimpanzees displayed large quantities of supragingival plaque, they had low bleeding scores. Peripheral blood neutrophils responded to innate and adaptive immune stimuli. In the follow up period two animals died and post mortem confirmed heart disease. Levels of NT-proBNP were found to be high in chimpanzees that died from heart disease. CONCLUSIONS: Whilst there appeared to be a correlation between probing depth and age, there appeared to be no correlation between dental data and heart data in this cohort.

Assessing the Educational Value of a Zoo Placement for Veterinary Students: A Report on Student Feedback and Perceptions.

Zoological medicine is an expanding field with limited practical training opportunities for veterinary students. Those training programs that do exist require significant financial and resource investment by both veterinary schools and the zoological organizations involved. This article summarizes the findings of a retrospective survey of students carried out to ascertain the educational value of a compulsory 5-day-long zoo clinical placement for final-year veterinary students. We aimed to explore the placement's potential impact on students' knowledge and attitudes toward zoological medicine and the role of modern zoos and conservation. Data were collected by means of an end-of-placement questionnaire (N = 200) and statistically analyzed for pre- versus post-placement changes and the effect of pre-placement interest and experience on student responses. Despite the placement's short time frame and lack of opportunity for in-depth comprehensive training in zoological medicine, students reported that the placement had a positive educational impact. More than 90% of students stated that their understanding about modern zoos was good or excellent at the end of the placement (compared with 35.0% before the placement), and 43.0% reported that the placement had a positive impact on their attitudes toward zoos. Students self-reported an increased understanding of the work of zoo clinicians, and there was a highly significant positive change in the students' reported opinions regarding wildlife conservation in general. We provide preliminary evidence to suggest that even short-duration but immersive zoo-based practical training has positive educational value for veterinary students.

Avian anaesthesia related mortality and the associated risk factors in a UK zoological collection.

OBJECTIVE: To analyse avian anaesthesia-related mortality in a UK zoological collection over a 5-year period and identify risk factors for mortality. STUDY DESIGN: Retrospective cohort study. ANIMALS: A total of 135 individual birds across 37 species, anaesthetized during 206 events in a UK zoological collection between 1 January 2014 and 30 June 2019 (inclusive). METHODS: Anaesthesia records were reviewed and variables such as age, body condition, weight, sex, duration of anaesthesia and health status were collated. Anaesthesia-related mortality was defined as those deaths occurring during anaesthesia and up to 7 days postanaesthesia. Outcome was analysed using multivariable conditional logistic regression. Overall mortality was defined and included birds euthanised during anaesthesia for non-anaesthesia related reasons. Data were summarised as median (range). A value of p < 0.05 was considered significant. Relative risks and 95% confidence intervals (95% CI) were calculated for the association between risk factors and anaesthetic death where a statistically significant difference was found. RESULTS: The overall mortality rate was 10.19% (95% CI = 6.06-14.3%), while anaesthesia-related mortality was 3.88% (95% CI = 1.69-7.51%). Birds with an abnormal health status had a 15.53-fold (95% CI = 1.95-123.63) increased risk of death compared with those with a normal health status. The duration of anaesthesia was also a statistically significant risk factor (p = 0.021) in the univariable analysis, but not when combined with health status. No other variables were associated with anaesthesia-related mortality. CONCLUSIONS AND CLINICAL RELEVANCE: Abnormal health status and longer anaesthetic procedures were associated with a significantly increased risk of anaesthesia-related death in this population of birds. It is recommended that anaesthetic duration is minimized, and pre-existing diseases are diagnosed where possible prior to general anaesthesia of birds. Anaesthetizing healthy birds was associated with a low risk of mortality.

Evaluation of the agreement of two oscillometric blood pressure devices with invasive blood pressure in anaesthetized chimpanzees (Pan troglodytes).

OBJECTIVE: To evaluate the agreement of two noninvasive blood pressure devices: a human device with the cuff placed on the wrist (Omron R1) and a veterinary device with the cuff placed on the upper brachium (Surgivet Advisor Vital Signs Monitor) with invasive blood pressure (IBP) measurement in anaesthetized chimpanzees. STUDY DESIGN: Prospective clinical study. ANIMALS: A convenience sample of 11 adult chimpanzees undergoing anaesthesia for translocation and routine health checks. METHODS: Systolic (SAP) and diastolic arterial pressures (DAP) were continuously recorded via a transducer connected to a femoral artery cannula, and at 5 minute intervals from the two oscillometric devices. Agreement was explored using Bland-Altman analysis and bias defined as the mean difference between the two measurement methods. Spearman correlation coefficients were calculated. Significance was set at p < 0.05. RESULTS: Bias and standard deviation for the Surgivet compared with IBP were 8.6 ± 18 for SAP and 8.4 ± 9.9 for DAP, showing a significant underestimation of both variables. Limits of agreement (LOA) were from -27 to 44 for SAP and from -11 to 28 for DAP. Correlation coefficients between the Surgivet and IBP values were 0.86 for SAP and 0.85 for DAP (p < 0.0001). Bias and standard deviation for the Omron compared with the IBP were -21 ± 25 for SAP and -18 ± 15 for DAP, showing a significant overestimation of both variables. LOA were from -70 to -28 for SAP and from -47 to 11 for DAP. Spearman correlation coefficients between the Omron and IBP values were 0.64 for SAP and 0.72 for DAP (p < 0.0001). CONCLUSIONS AND CLINICAL RELEVANCE: Although neither device met all the criteria for device validation, the Surgivet presented better agreement with IBP values than the Omron in adult anaesthetized chimpanzees.

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.

Non-Infectious, Necrotizing and Granulomatous Aortitis in a Female Gorilla.

A 41-year-old female captive gorilla with progressive weight loss and hydrothorax of unknown origin was euthanized and submitted for necropsy. The ascending aorta showed intimal aortic thickenings, consistent with so called 'tree bark' changes. Microscopic examination revealed a non-infectious, necrotizing and granulomatous aortitis with no evidence of systemic vasculitis or infectious disease elsewhere in the body. While rare, large vessel vasculitides should be considered as a differential diagnosis in gorillas presenting with progressive non-specific signs and vascular intimal changes.

Discovery of os cordis in the cardiac skeleton of chimpanzees (Pan troglodytes).

Cardiovascular diseases, especially idiopathic myocardial fibrosis, is one of the most significant causes of morbidity and mortality in captive great apes. This study compared the structure and morphology of 16 hearts from chimpanzees (Pan troglodytes) which were either healthy or affected by myocardial fibrosis using X-ray microtomography. In four hearts, a single, hyperdense structure was detected within the right fibrous trigone of the cardiac skeleton. High resolution scans and histopathology revealed trabecular bones in two cases, hyaline cartilage in another case and a focus of mineralised fibro-cartilaginous metaplasia with endochondral ossification in the last case. Four other animals presented with multiple foci of ectopic calcification within the walls of the great vessels. All hearts affected by marked myocardial fibrosis presented with bone or cartilage formation, and increased collagen levels in tissues adjacent to the bone/cartilage, while unaffected hearts did not present with os cordis or cartilago cordis. The presence of an os cordis has been described in some ruminants, camelids, and otters, but never in great apes. This novel research indicates that an os cordis and cartilago cordis is present in some chimpanzees, particularly those affected by myocardial fibrosis, and could influence the risk of cardiac arrhythmias and sudden death.

Evaluation of relationships between results of electrocardiography and echocardiography in 341 chimpanzees (Pan troglodytes).

OBJECTIVE: To examine potential relationships between ECG characteristics and echocardiographic measures of cardiac structure in chimpanzees (Pan troglodytes). ANIMALS: 341 chimpanzees (175 males and 166 females) from 5 sanctuaries and 2 zoological collections. PROCEDURES: Chimpanzees were anesthetized for routine health examinations between May 2011 and July 2017 as part of the International Primate Heart Project and, during the same anesthetic events, underwent 12-lead ECG and transthoracic echocardiographic assessments. Relationships between results for ECG and those for echocardiographic measures of atrial areas, left ventricular internal diameter in diastole (LVIDd), and mean left ventricular wall thicknesses (MLVWT) were assessed with correlational analysis, then multiple linear regression analyses were used to create hierarchical models to predict cardiac structure from ECG findings. RESULTS: Findings indicated correlations (r = -0.231 to 0.310) between results for ECG variables and echocardiographic measures. The duration and amplitude of P waves in lead II had the strongest correlations with atrial areas. The Sokolow-Lyon criteria, QRS-complex duration, and R-wave amplitude in leads V6 and II had the strongest correlations with MLVWT, whereas the Sokolow-Lyon criteria, QRS-complex duration, and S-wave amplitude in leads V2 and V1 had the strongest correlations with LVIDd. However, the ECG predictive models that were generated only accounted for 17%, 7%, 11%, and 8% of the variance in the right atrial end-systolic area, left atrial end-systolic area, MLVWT, and LVIDd, respectively. CONCLUSIONS AND CLINICAL RELEVANCE: Results indicated that relationships existed between ECG findings and cardiac morphology in the chimpanzees of the present study; however, further research is required to examine whether the predictive models generated can be modified to improve their clinical utility.

Comparison of 25-hydroxyvitamin D concentration in chimpanzee dried blood spots and serum.

BACKGROUND: Dried blood spots (DBS) are used in human medicine to measure total 25-hydroxyvitamin D (25-OHD) in the blood. However, this easy and affordable sampling technique has not been evaluated in primates to measure vitamin D concentrations. OBJECTIVES: We aimed to compare 25-OHD measurements in chimpanzee serum at two different laboratories and determine the precision and accuracy of the DBS method by comparing DBS and serum results. METHODS: Blood samples from 17 captive chimpanzees were collected, and 25-OHD3 and 25-OHD2 were measured in serum at two accredited laboratories using liquid chromatography-tandem mass spectrometry. The same analytes were measured on DBS cards, and results were compared with that of serum. Data were assessed using the Spearman correlation, Deming regression, and Bland-Altman analyses. RESULTS: The correlation coefficient between the two measurements in serum was rs  = .51 (P = .04), and the mean bias was -1.25 ± 14.83. When comparing 25-OHD concentrations measured in DBS and serum at the same laboratory, the rs was 0.7 (P = .002), and the mean bias was 1.42 ± 14.58. Estimated intra-assay and inter-assay coefficients of variation for DBS results were 6% and 12.6%, respectively. CONCLUSIONS: Although substantial analytical variability was found in 25-OHD measurements regardless of the sample type, the identification of both constant and proportional error and wider limits of agreement with the DBS technique makes the interpretation of DBS results challenging, especially for values close to clinical cut-off points. The DBS and serum methods were not interchangeable, and further studies are needed to validate DBS samples for vitamin D measurements in chimpanzees.

Idiopathic Myocardial Fibrosis in Captive Chimpanzees (Pan troglodytes).

Cardiovascular disorders and predominantly idiopathic myocardial fibrosis are frequently associated with mortality among zoo-housed chimpanzees (Pan troglodytes). Formalin-fixed whole hearts of deceased chimpanzees housed in zoos (n = 33) and an African sanctuary (n = 2) underwent detailed macroscopic and histopathologic examination using a standardized protocol. Archived histological slides from the hearts of 23 additional African sanctuary-housed chimpanzees were also examined. Myocardial fibrosis (MF) was identified in 30 of 33 (91%) of the zoo-housed chimpanzees but none of the 25 sanctuary-housed chimpanzees. MF was shown to be characterized by both interstitial and replacement fibrosis. Immunophenotyping demonstrated that the fibrotic lesions were accompanied by the increased presence of macrophages, alpha smooth muscle actin-positive myofibroblasts, and a minimal to mild T-cell-dominant leukocyte infiltration. There was no convincing evidence of cardiotropic viral infection or suggestion that diabetes mellitus or vitamin E or selenium deficiency were associated with the presence of the lesion. However, serum vitamin D concentrations among zoo-housed chimpanzees were found to be lower in seasons of low ultraviolet light levels.

Cardiac structure and function characterized across age groups and between sexes in healthy wild-born captive chimpanzees (Pan troglodytes) living in sanctuaries.

OBJECTIVE: To comprehensively characterize cardiac structure and function, from infancy to adulthood, in male and female wild-born captive chimpanzees (Pan troglodytes) living in sanctuaries. ANIMALS: 290 wild-born captive chimpanzees. PROCEDURES: Physical and echocardiographic examinations were performed on anesthetized chimpanzees in 3 sanctuaries in Africa between October 2013 and May 2017. Results were evaluated across age groups and between sexes, and potential differences were assessed with multiple 1-way independent Kruskal-Wallis tests. RESULTS: Results indicated that left ventricular diastolic and systolic function declined at a younger age in males than in females. Although differences in right ventricular diastolic function were not identified among age groups, right ventricular systolic function was lower in adult chimpanzees (> 12 years old), compared with subadult (8 to 12 years old) and juvenile (5 to 7 years old) chimpanzees. In addition, male subadult and adult chimpanzees had larger cardiac wall dimensions and chamber volumes than did their female counterparts. CONCLUSIONS AND CLINICAL RELEVANCE: Results of the present study provided useful reference intervals for cardiac structure and function in captive chimpanzees categorized on the basis of age and sex; however, further research is warranted to examine isolated and combined impacts of blood pressure, age, body weight, and anesthetic agents on cardiac structure and function in chimpanzees.