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.

Survey of Behavioral Indices of Welfare in Research Chimpanzees (Pan troglodytes) in the United States.

Chimpanzees demand specialized housing and care and the highest degree of attention to animal welfare. The current project used a survey method to collate information on chimpanzee housing and behavioral indices of welfare across all 6 of the chimpanzee research facilities in the United States. Data were compiled on 701 chimpanzees ranging from 2 to 62 y old (mean age, 26.0 y). All chimpanzees except for one were socially housed; the median group size was 7 animals, and group sizes ranged from 1 to 14. All of the subjects had access to outdoor spaces each day. Daily access to a natural substrate in the chimpanzee's enclosure was available for 63.8% of the subjects. Overall, 94.1% of the chimpanzees used tools to acquire food, 48.1% built nests, 75.8% copulated, and 83.3% initiated grooming bouts. The following atypical behaviors were reported most often: rocking (13.0%), coprophagy (10.0%), and stereotyped behaviors other than rocking (9.4%). There was widespread evi- dence of positive animal training techniques, with nearly all (97.7%) subjects reported to generally voluntarily cooperate with shifting in their enclosure, and 72.2% were reported to present for an injection of anesthetic. We include some comparison between these findings and data describing zoo-housed chimpanzees. In addition, we discuss survey findings in reference to recommendations made by the NIH Working Group on the Use of Chimpanzees in NIH-supported Research. The current survey assessed a larger sample of chimpanzees living under human care than has been published previously. This broad analysis can help to guide future improvements in behavioral management to address behavioral problems or deficits.

Echocardiography parameters of clinically normal adult captive chimpanzees (Pan troglodytes).

OBJECTIVE: To generate reference ranges for echocardiographic variables in clinically normal adult chimpanzees (Pan troglodytes). DESIGN: Retrospective cohort study. ANIMALS: 88 clinically normal adult chimpanzees. PROCEDURES: Echocardiographic data obtained between 2002 and 2011 from chimpanzees at the Alamogordo Primate Facility were reviewed (263 echocardiograms obtained from 158 individuals). Data from clinically normal individuals (33 females and 55 males) were analyzed. Basic cardiac parameters measured in all individuals included aortic root diameter and left atrial diameter in the short and long axis during diastole. Left ventricular measurements included left ventricular internal diameter in systole and diastole and diastolic septal and posterior wall thickness. The E point to septal separation was also measured. Spectral Doppler measurements included the peak flow velocity of the pulmonary artery and aorta and diastolic transmitral flow. The presence of arrhythmias was also noted. RESULTS: Standard echocardiographic findings for a large group of adult female and male chimpanzees were obtained. Female and male chimpanzees were grouped by age in 10-year blocks, and echocardiographic findings were analyzed statistically by 10-year block. In male chimpanzees, cardiac arrhythmias were noted to increase with age. CONCLUSIONS AND CLINICAL RELEVANCE: Cardiovascular disease is an important cause of morbidity and death in captive chimpanzees; however, basic echocardiographic measurements from a large cohort of clinically normal animals have not previously been reported. The number of animals in the present study was insufficient to generate reference ranges; however, data from a large cohort of clinically normal animals are presented. This information will be useful for veterinarians working in clinical and research settings with this species.

Hypertension increases with aging and obesity in chimpanzees (Pan troglodytes).

Cardiovascular disease is a primary cause of morbidity and mortality in captive chimpanzees. Four years of blood pressure (BP) data were analyzed from a captive former laboratory population of 201 healthy adult chimpanzees with assessment of age and obesity on elevated BP. Five different measures of obesity were compared: abdominal girth, basal metabolic rate, body-mass index (BMI), body weight, and surface area. Systolic BP varied by sex. Obesity did not influence male BP. For females, obesity was a significant determinant of BP. The best measure of female obesity was basal metabolic rate and the worst was BMI. Median systolic BP of healthy weight females (<54.5 kg) was significantly lower (128 mmHg) than overweight or obese females (140 mmHg), but both were lower than all males (147 mmHg). For diastolic BP, neither sex nor any of the five obesity measures was significant. But age was highly significant, with geriatric chimpanzees (>30 years) having higher median diastolic BP (74 mmHg) than young adults of 10-29 years of age (65 mmHg). By these criteria, 80% of this population is normotensive, 7% prehypertensive, and 13% hypertensive. In summary, systolic BP intervals required adjustment for obesity among females but not males. Diastolic BP required adjustment for advanced age (≥30 years). Use of these reference intervals can facilitate timely clinical care of captive chimpanzees.

Chronic diseases in captive geriatric female Chimpanzees (Pan troglodytes).

The current aging population of captive chimpanzees is expected to develop age-related diseases and present new challenges to providing their veterinary care. Spontaneous heart disease and sudden cardiac death are the main causes of death in chimpanzees (especially of male animals), but little is known about the relative frequency of other chronic diseases. Furthermore, female chimpanzees appear to outlive the males and scant literature addresses clinical conditions that affect female chimpanzees. Here we characterize the types and prevalence of chronic disease seen in geriatric (older than 35 y) female chimpanzees in the colony at Alamogordo Primate Facility. Of the 16 female chimpanzees that fit the age category, 87.5% had some form of chronic age-related disease. Cardiovascular-related disease was the most common (81.25%) followed by metabolic syndrome (43.75%) and renal disease (31.25%). These data show the incidence of disease in geriatric female chimpanzees and predict likely medical management challenges associated with maintaining an aging chimpanzee population.

Use of an implantable loop recorder in the investigation of arrhythmias in adult captive chimpanzees (Pan troglodytes).

Cardiovascular disease in general, and cardiac arrhythmias specifically, is common in great apes. However, the clinical significance of arrhythmias detected on short-duration electrocardiograms is often unclear. Here we describe the use of an implantable loop recorder to evaluate cardiac rhythms in 4 unanesthetized adult chimpanzees (Pan troglodytes), 1 with a history of possible syncope and 3 with the diagnosis of multiform ventricular ectopy (ventricular premature complexes) and cardiomyopathy. The clinical significance of ventricular ectopy was defined further by using the implantable loop recorder. Arrhythmia was ruled out as a cause of collapse in the chimpanzee that presented with possible syncope because the implantable loop recorder demonstrated normal sinus rhythm during a so-called syncopal event. This description is the first report of the use of an implantable loop recorder to diagnose cardiac arrhythmias in an unanesthetized great ape species.

Effects of aging and blood contamination on the urinary protein-creatinine ratio in captive chimpanzees (Pan troglodytes).

The initial goal of this study was to evaluate proteinuria by using the protein to creatinine (UPC) ratio of urine obtained by cystocentesis of healthy adult captive chimpanzees. Urine samples were collected by using ultrasound-guided cystocentesis from 125 (80 male, 45 female) captive chimpanzees. All samples were collected over a 17-mo time period (August 2008 to January 2010) during the animal's annual physical examination. Samples were assayed at a veterinary diagnostic laboratory. Results indicated that both age and blood contamination affect the UPC ratio and therefore alter the diagnostic utility of the UPC ratio in chimpanzees. In addition, this research establishes reference ranges by age for the UPC ratio in healthy adult chimpanzees. Chimps younger than the median age of 24.6 y have a median UPC ratio of 0.098 (range, 0 to 1.76), whereas older animals have a median UPC of 0.288 (range, 0 to 2.44). Our results likely will enable veterinarians working with chimpanzees to better evaluate their renal function.

Association of brain-type natriuretic protein and cardiac troponin I with incipient cardiovascular disease in chimpanzees (Pan troglodytes).

Cardiovascular disease (CVD) is the primary cause of morbidity and mortality in chimpanzees, but its etiology and clinical presentations remain poorly understood. The disease in chimpanzees differs sufficiently from that in humans that simple extrapolation from human findings are inadequate to guide clinical diagnoses. Nevertheless, the burden of disease posed by CVD made it important to attempt to identify specific chimpanzees at risk of developing CVD to allow clinical intervention prior to clinical presentation of advanced disease. We screened 4 CVD biomarkers used in human and veterinary medicine to identify markers with prognostic value in chimpanzees. Biomarkers included complete lipid panel, C-reactive protein, brain-type natriuretic protein, and cardiac troponin I. Serum levels of brain-type natriuretic protein differed between chimpanzees with CVD and heart-healthy controls. Cardiac troponin I gave mixed results. C-reactive protein and lipid panel values were not informative for cardiovascular disease, although total cholesterol, LDL-cholesterol, and triglycerides increased significantly with decade of life. Values of braintype natriuretic protein exceeding 163 mg/mL had a specificity of 90.5% for CVD, whereas levels of cardiac troponin I above the threshold of detection (0.20 ng/mL) appeared to be clinically relevant. More extensive clinical studies are recommended to validate these specific values. We conclude that brain-type natriuretic protein and possibly cardiac troponin I are useful diagnostic biomarkers for incipient CVD processes in chimpanzees.

Diagnosis and treatment of degenerative joint disease in a captive male chimpanzee (Pan troglodytes).

Degenerative joint disease (DJD), also known as osteoarthritis, has been well documented in aging populations of captive and free-ranging macaques; however, successful treatments for DJD in nonhuman primates have not been published. Published data on chimpanzees show little to no DJD present in the wild, and there are no published reports of DJD in captive chimpanzees. We report here the first documented case of DJD of both the right and left femorotibial joints in a captive male chimpanzee. Progression from minimal to moderate to severe osteoarthritis occurred in this animal over the course of 1 y. Treatment with chondroprotective supplements (that is, glucosamine chondroitin, polysulfated glycosaminoglycan) and intraarticular corticosteroid injections (that is, methylprednisolone, ketorolac), together with pain management (that is, celecoxib, tramadol, carprofen), resulted in increased activity levels and decreased clinical signs of disease. DJD has a considerable negative effect on quality of life among the human geriatric population and therefore is likely to be one of the most significant diseases that will affect the increasingly aged captive chimpanzee population. As this case study demonstrates, appropriate treatment can improve and extend quality of life dramatically in these animals. However, in cases of severe osteoarthritis cases, medication alone may be insufficient to increase stability, and surgical options should be explored.

Use of biomarkers of collagen types I and III fibrosis metabolism to detect cardiovascular and renal disease in chimpanzees (Pan troglodytes).

Cardiovascular disease is the leading cause of morbidity and mortality among captive chimpanzees. The most prevalent form of cardiovascular disease among chimpanzees is sudden cardiac death. Myocardial fibrosis was the only significant pathologic lesion observed in affected animals at necropsy. We previously showed an association between myocardial fibrosis and sudden cardiac death. The presumed pathogenesis was interstitial myocardial fibrosis that led to decreased myocardial contractility and interrupted signal propagation in the heart, leading to fibrillation and resulting in sudden cardiac death. In this pilot study, we assayed 5 biomarkers of collagen types I and III metabolism and fibrogenesis and studied their association with CVD in chimpanzees. The biomarker MMP1 did not crossreact in chimpanzee sera and could not be studied further. Two biomarkers (TIMP1 and PINP) and their difference showed no significant association with CVD in chimpanzees. The biomarkers ICTP and PIIINP were significantly increased in cases of CVD with concurrent renal disease. Furthermore, both biomarkers showed a significant trend to increase with disease severity. We conclude that ICTP and PIIINP warrant further study for antemortem detection of renal and myocardial fibrosis in chimpanzees.

Diagnosis and treatment of pulmonary arterial hypertension and atrial fibrillation in an adult chimpanzee (Pan troglodytes).

This report describes the diagnosis and treatment of pulmonary arterial hypertension (PAH) in an adult male captive chimpanzee. Although cardiovascular disease in general is common in human and great apes, diagnosis and treatment of PAH in nonhuman primates are uncommon. In the case we present, the adult chimpanzee was diagnosed with an arrhythmia during an annual physical examination and later with PAH during a scheduled cardiovascular evaluation. PAH can either be primary or secondary and can lead to right ventricular overload and heart failure. This description is the first case study of pulmonary arterial hypertension in a great ape species.

Interstitial myocardial fibrosis in a captive chimpanzee (Pan troglodytes) population.

The clinical and necropsy records of 36 (25 male and 11 female) chimpanzees age 10 to 40 y old that died over a 6-y period (2001 to 2006) were reviewed. All animals had annual physical exams that included electrocardiograms and serial blood pressures. Nine of the 36 animals had a complete cardiac evaluation by a board certified veterinary cardiologist, and 7 of the 36 animals (19%) were diagnosed with some form of cardiomyopathy. Systemic hypertension was noted in 3 cases. Cardiac arrhythmias (ventricular ectopy) were seen in 15 (12 male and 3 female) of the 36 animals (42%). Sudden cardiac death (SCD) occurred in 13 (11 male and 2 female) chimps (36%) and was the leading cause of death (n = 13), followed by renal failure (n = 9) and septicemia (n = 3). Histologic examination of the hearts revealed interstitial myocardial fibrosis (IMF) in 29 chimpanzees (81%), and all of the animals that died suddenly due to cardiac causes had IMF to varying degrees. More data will be needed to identify the possible causes of IMF in captive chimpanzees, and IMF may be associated with arrhythmias and SCD in these animals.

Sudden cardiac death in 13 captive chimpanzees (Pan troglodytes).

Sudden cardiac death (SCD), presumed secondary to fatal arrhythmias, is a common cause of mortality in captive chimpanzees at the Alamogordo Primate Facility. Over the 6-year period at the Alamogordo Primate Facility between 2001 and 2006, 13 animals were defined as sudden cardiac death (11 male and 2 female) on the basis of clinical presentation which was 38% of all deaths. All animals had annual physical exams, including electrocardiograms and serial blood pressures. Six of the 13 animals underwent a complete cardiac evaluation by a veterinary cardiologist and all six of these animals were diagnosed with various degrees of cardiomyopathy. Systemic hypertension was noted in two of the 13 cases and antemortem cardiac arrhythmias were seen in all 13 animals. Histological examination of the hearts revealed myocardial fibrosis in 12 chimpanzees. Most of the animals (10/13) that died of sudden cardiac death had cardiomegaly (increased heart weight/body weight ratio) and some degree of myocardial fibrosis noted. Additional data as well as serial diagnostic evaluations will be needed to identify the possible causes of sudden cardiac death in captive chimpanzees.