Abstract
During 1990–2003, 94 chimpanzees (Pan troglodytes) died in zoos that are currently accredited by the American Zoo and Aquarium Association (AZA). Not all institutions were AZA members during the time period evaluated. However, all deaths from each institution were included to provide a more robust database.
In 2003, complete gross and histopathology reports were requested from the holding institutions by the Chimpanzee Species Survival Plan (SSP)® Veterinary Advisor. Limited medical history was requested for individuals where illness was directly associated with death. All 94 records were retrieved for a 100% survey return rate; however, the depth of reporting varied across the database (Table 1).
Table 1. Pathology reporting for
chimpanzee mortalities (1990–2003)
Full report
|
40
|
Gross only
|
12
|
Histopathology only
|
2
|
Medical records only
|
35
|
Death report only
|
5
|
Total
|
94
|
Methods
Each report was reviewed for signalment (specimen gender and age at death), medical history at death, primary cause of death, and secondary pathologic findings. Primary causes of death and secondary pathologic findings were categorized by body system (cardiopulmonary, endocrine, gastrointestinal, integument, lymphatic, musculoskeletal, nervous, reproductive, urinary) and representative pathologic process (degenerative, anomalous, metabolic, neoplastic, infectious/inflammatory, toxic, traumatic).
Of the 94 animals, 22 (7.9.6, 23%) were neonates (≤1 day of age), of which 10 (6.2.2, 45%) were stillborn, 17 (8.9, 18%) were infants (1 day to 1 year of age), 20 (10.10, 21%) were juveniles (1–10 years of age), 8 (5.3, 9%) were young adults (10–20 years of age), 16 (4.12, 17%) were mature adults (20–35 years of age), and 11 (3.8, 12%) were elderly adults (>35 years of age). The primary cause of death is presented by age categories and representative pathologic process. Specific primary etiologies are provided separately (Table 2). Secondary or incidental findings were too numerous to be effectively tabulated. However, certain pathologic trends were observed.
Table 2. Primary cause of death by age class for chimpanzee mortalities (1990–2003)
Cause of death
|
<1 day
|
<1 day–>1 y
|
1–10 y
|
10–35 y
|
>35 y
|
Conspecific trauma
|
4
|
3
|
3
|
0
|
0
|
Trauma
|
2
|
1
|
1
|
1
|
0
|
Premature birth
|
3
|
0
|
0
|
0
|
0
|
Malpositioning
|
1
|
0
|
0
|
0
|
0
|
Failure to thrive
|
0
|
1
|
0
|
0
|
0
|
Spina bifida
|
0
|
1
|
0
|
0
|
0
|
Cerebral amoebiasis
|
0
|
0
|
1
|
0
|
0
|
Noninfectious CNS disease
|
0
|
1
|
1
|
0
|
0
|
Diabetes insipidus
|
0
|
0
|
1
|
0
|
0
|
Clostridial enteritis
|
0
|
0
|
1
|
0
|
0
|
Internal abdominal abscess
|
0
|
0
|
0
|
2
|
0
|
Glossal actinomycosis
|
0
|
0
|
0
|
1
|
0
|
Systemic amyloidosis
|
0
|
0
|
0
|
1
|
0
|
Systemic Coccidiodes
|
0
|
0
|
0
|
0
|
1
|
Disseminated granulomatosis
|
0
|
0
|
0
|
0
|
1
|
Chronic renal disease
|
0
|
0
|
1
|
3
|
0
|
Acute renal failure
|
0
|
0
|
0
|
0
|
1
|
Noninfectious cardiac disease
|
0
|
0
|
0
|
5
|
2
|
Aneurysm
|
0
|
0
|
0
|
0
|
2
|
Respiratory failure
|
0
|
0
|
0
|
1
|
0
|
Encephalomyocarditis
|
0
|
0
|
1
|
0
|
0
|
Aspiration pneumonia
|
0
|
0
|
1
|
1
|
0
|
Infectious pneumonia
|
0
|
4
|
0
|
0
|
1
|
Metabolic bone disease
|
0
|
0
|
1
|
0
|
0
|
Hepatocellular carcinoma
|
0
|
0
|
0
|
2
|
1
|
Autolysis
|
1
|
2
|
0
|
0
|
0
|
Exhibit relateda
|
0
|
0
|
4
|
6
|
1
|
Unknown
|
11
|
4
|
4
|
1
|
1
|
Totals
|
22
|
17
|
20
|
24
|
11
|
Results and Discussion
Cardiovascular disease was identified as an important cause of disease in chimpanzees, particularly for adults (27 of 35 animals, 77%) (Table 3). This is also a disease concern reported in captive gorillas (Gorilla gorilla).3 Intra-abdominal abscessation, recently reported as a serious disease process in gorilla, was not a notable finding in chimpanzee mortalities.2 Parasitism was identified frequently antemortem, with Balantidium coli identified as an endemic parasite of minimal pathogenicity, except at times of stress, from a survey of 35% of AZA-accredited institutions (n=40) currently housing chimpanzees.1 B. coli was similarly the most often observed parasite postmortem. Parasitism itself was secondarily reported in only 16% of all chimpanzee mortalities (Table 4). Identified at nearly the same frequency of affected individuals, neoplasia was identified in 15% of the chimpanzees (Table 5). This pathology was exclusively identified in animals greater than 10 years with a mean of 32.7 years of age. Exhibit-related mortalities included drowning (n=7), post-escape recovery efforts (n=3), and entrapment in an exhibit prop (n=1), or 12% of the total deaths, with an average age of 15.2 years of age (range=15 months to 37 years). As the predominant cause in this category was drowning, the current Chimpanzee SSP® recommendation against water moats as primary containment was supported.
Table 3. Types of cardiovascular disease by age for chimpanzee mortalities (1990–2003)
Cardiovascular disease
|
<1 day–>1 y
|
1–10 y
|
10–35 y
|
>35 y
|
Congestive heart failure
|
0
|
0
|
1a
|
1a
|
Endocardiosis
|
0
|
0
|
3
|
3
|
Myocardial fibrosis
|
0
|
1
|
9a
|
4a
|
Atherosclerosis
|
0
|
0
|
1
|
1
|
Arteriosclerosis
|
0
|
0
|
1
|
1
|
Viral myocarditis
|
1
|
1a
|
1
|
0
|
Aortic aneurysm
|
0
|
0
|
0
|
1a
|
aPrimary lesions in cardiovascular disease were found in congestive heart failure (10–35 y, n=1; >35 y, n=1), aneurysm (>35 y, n=1), myocardial fibrosis (10–35 y, n=4; >35 y, n=1), and viral myocarditis (1–10 y, n=1)
Table 4. Internal parasites identified at pathologic review of chimpanzees (1990–2003)
Parasite
|
Location
|
Incidences
|
Balantidium coli
|
Small/large intestine
|
6
|
Enterobius sp.
|
Large intestine
|
4
|
Trichuris sp.
|
Intestine
|
1
|
Cryptosporidia sp.
|
Large intestine
|
2
|
Nematode, unidentified
|
Small/large intestine
|
3
|
Ciliate, unidentified
|
Intestine
|
1
|
Amoeba, unidentifieda
|
Brain
|
1
|
aThis parasite was the primary cause of animal’s death, rather than an incidental finding
Table 5. Types of neoplasia identified for chimpanzee mortalities (1990–2003)
Neoplasia
|
Organ
|
Metastasisa
|
Age
|
1° vs 2°b
|
Carcinoma
|
Liver
|
N
|
10 y
|
1°
|
Carcinoma
|
Liver
|
N
|
31 y
|
2°
|
Carcinoma
|
Unidentified
|
Y
|
39 y
|
1°
|
Carcinoma
|
Unidentified
|
Y
|
43 y
|
2°
|
Leiomyoma
|
Uterus
|
N
|
35 y
|
2°
|
Leiomyoma
|
Uterus
|
N
|
47 y
|
2°
|
Leiomyoma
|
Uterus
|
N
|
43 y
|
2°
|
Adenoma
|
Liver
|
N
|
13 y
|
2°
|
Adenoma
|
Intestinal tract
|
N
|
37 y
|
2°
|
Fibroma
|
Uterus
|
N
|
28 y
|
2°
|
Fibroma
|
Uterus
|
N
|
36 y
|
2°
|
Lipoma
|
Fat
|
N
|
23 y
|
2°
|
Lipoma
|
Fat
|
N
|
36 y
|
2°
|
Adenoma
|
Cervix
|
N
|
37 y
|
2°
|
aN (metastasis not observed), Y (metastasis observed)
b1° (primary cause of death), 2° (secondary/incidental finding)
The summary of this information will contribute to the development of differential diagnoses for presented clinical cases. Adjustments to medical management can be made from the determination of the more common causes of death. Assessment of necropsies from the captive population will provide a comparative database for those performed in wild populations. To extend the utility of this evaluation, continued updates will be generated for the Chimpanzee SSP® annual report using these parameters for consistency.
Acknowledgments
The authors appreciate the cooperation of the following institutions’ veterinary staffs in providing the records for this review: North Carolina Zoological Park (Asheboro, NC), Gladys Porter Zoo (Brownsville, TX), Busch Gardens (Tampa, FL), Lincoln Park Zoo (Chicago, IL), Cleveland Metroparks Zoo (Cleveland, OH), Cheyenne Mountain Park Zoo (Colorado Springs, CO), Dallas Zoo (Dallas, TX), Detroit Zoo (Detroit, MI), Sequoia Park (Eureka, CA), Fort Worth Zoological Park (Fort Worth, TX), Chaffee Zoo (Fresno, CA), Hogle Zoo (Salt Lake City, UT), Jackson Zoological Park (Jackson, MS), Kansas City Zoological Park (Kansas City, MO), Knoxville Zoo (Knoxville, TN), Little Rock Zoo (Little Rock, AR), Los Angeles (Los Angeles, CA), Henry Vilas Zoo (Madison, WI), Sunset Zoo (Manhattan, KS), Montgomery Zoo (Montgomery, AL), Oakland Zoo (Oakland, CA), Metroparks Zoo (Portland, OR), Sacramento Zoo (Sacramento, CA), Riverside Zoo (Scottsbluff, NE), Sedgwick County Zoo (Wichita, KS), Saint Louis Zoo (St. Louis, MO), Toledo Zoological Gardens (Toledo, OH), Tulsa Zoo and Living Museum (Tulsa, OK), and Lion Country Safari (Loxahatchee, FL).
Literature Cited
1. Backues, K., and K.C. Gamble. 2003. Chimpanzee SSP® Veterinary Advisor Parasite Survey.
2. Schulman, F.Y., A. Farb, R. Virmani, and R.J. Montali. 1995. Fibrosing cardiomyopathy in captive western lowland gorillas (Gorilla gorilla gorilla) in the United States: a retrospective study. J. Zoo Wildl. Med. 26(1): 43–51.
3. Mylniczenko, N.D. 2003. A preliminary report on intra-abdominal abscesses in captive western lowland gorillas (Gorilla gorilla gorilla). Proc. Am. Assoc. Zoo Vet.: 62–65.