Abstract

Captive western lowland gorillas (Gorilla gorilla gorilla) have a high prevalence of intra-abdominal abscesses when compared to other reported diseases in this species. A database was created from medical records obtained from North American zoos to investigate possible etiologies. The goals were to 1) evaluate methods used to diagnose abscesses, 2) establish prognostic and risk factors, 3) determine etiologies, and 4) evaluate treatment strategies. This report presents the initial results of the study.

Introduction

While it is not surprising that gorillas develop intra-abdominal abscesses, there appears to be an abnormally high prevalence in captive animals with considerable morbidity and mortality in an unpublished examination of captive gorilla records. Reviews of gorilla diseases have not reported any cases of intra-abdominal abscesses.^4-8,12,13 Gastrointestinal disease is often cited as one of the top three medical problems in gorillas and includes peritonitis, ulcerative colitis, and parasitism; however, severity of disease is rarely mentioned and abscess formation is not reported.

Intra-abdominal abscesses have been reported in both exotic and domestic species including a chimpanzee.^1,3,6,9,15 The frequent occurrence of abdominal abscesses in humans is well documented in the literature. Common causes include a ruptured appendix, intestinal parasitism (Entamoeba histolytica), perforating ulcers, pelvic inflammatory disease, and sequelae to abdominal surgery.¹¹¹⁶

A differential list of diagnoses for intra-abdominal abscesses in gorillas includes 1) organ perforation due to a) foreign body trauma, b) parasitic, bacterial, viral, and toxic enteritis, c) reproductive tract infection; 2) iatrogenic causes: infection or foreign body introduction secondary to surgery; and 3) nutritional deficiencies leading to poor intestinal mucosal integrity (e.g., low fiber content of diet).¹⁰

Methods

Medical and necropsy records were requested for normal and clinically ill animals from American Zoo and Aquarium Association (AZA) accredited zoos in North America. Animal identification was based on the studbook number. Animals without a studbook number were assigned a unique number, which would not conflict with legitimate studbook numbers. A database was created using a relational database (Microsoft Access; Microsoft Corporation, One Microsoft Way Redmond, WA, USA) that can accommodate complex medical record information. An ‘event’ table was created to record major occurrences in an animal's record, for example, severe dental tartar would be a 'disease' event. Additional tables were used to record details specific to different types of events, including anesthesia, physical examination, disease diagnosis, parturition, vaccination, parasitology, bloodwork (CBC, serum chemistry, viral titers), urinalysis, surgery, microbiologic culture, pathology, treatment, and other diagnostics. An animal was classified as having an intra­abdominal abscess if there was gross or histologic diagnosis of purulent material and inflammation of tissue in the abdominal cavity.

Results

Prevalence

The 2000 North American gorilla studbook lists 1,462 animals (live and dead) with assigned studbook numbers. Of these, 712 (49%) could be tracked and potentially had a medical record. Three hundred and seven (43%) partial or complete files were collected from 35 participating institutions for this project. Records were collected from August 1969 to early 2002. Gender distribution was 152 (49.5%) females, 153 (49.8%) males, and 2 (006%) unknown.

Twenty-six animals had suspected intra-abdominal abscesses. Of these, 21 records were available to the author. All 21 were subsequently confirmed to have abscesses. The population of animals confirmed to have abscesses was predominantly female (90%), typically 17–36 yr of age, obese (72–140 kg) and reproductively inactive.

Clinical History

Clinical signs in all cases included lethargy and anorexia. Rectogenital discharge, constipation, abdominal distension, and vomition were occasionally reported. Less frequently noted were diarrhea, trembling, and weakness. Clinical symptoms were often present weeks to months prior to confirming a diagnosis of intra-abdominal abscess. Several animals had reproductive exams involving an invasive procedure (laparoscopy or uterine flush with contrast) prior to abscess formation.

Diagnostics

Diagnostics most often performed were bloodwork, abdominal radiography (survey and contrast), abdominal ultrasound, fluoroscopy, gallium scan, computed tomography (CT scan), ultrasound­guided percutaneous fine needle aspiration, culture of the abscess, and surgical exploration. Abdominal palpation was not a good indicator of the presence of an abscess. Challenges to making a diagnosis included concurrent disease, early stage of abscess formation, and poor quality of imaging studies. In every case human physicians were consulted.

Initial Results

Abscess origin was frequently difficult to ascertain due to severe adhesion formation. The colon and reproductive organs were often incorporated within a fibrous mat, which occasionally involved the urinary tract organs. Fistulas were a common occurrence and often drained perirectally or perivaginally. Intestinal perforations, including the appendix in two cases, were documented, although in many circumstances perforations were suspected but could not be confirmed due to adhesions. Specific muscles (rectus abdominus, coccygeal muscles, and the psoas muscles) were occasionally associated with abscesses, but this was not typically documented in the medical record. Plant material foreign bodies were an additional finding and, in some instances, were posited as the causative agent. Several animals had purulent material free in the coelomic cavity.

Bacteria cultured from abscesses included Escherichia coli, Morganella morganii, Fusobacterium necrophorum, Bacteroides sp., hemolytic Streptococcus and Staphylococcus spp., Enterococcus sp., Hemophilus sp., Actinomyces sp., Proteus sp. and Klebsiella pneumoniae. The protozoan Balantidium coli. was found in fecal exams and biopsies of intestinal mucosa in many animals with abscesses. While this organism can cause pathology in gorillas,¹⁸ its relevance in abscess formation is unclear.

Treatment

Treatment included multimodal long-term antibacterial therapy and analgesics in all cases. Additional treatments included antifungal therapy, gastric protective drugs (H2 blockers, proton pump inhibitors), peritoneal lavage, surgical debridement, surgical resection of portions of the intestinal or reproductive tract, and antibiotic-impregnated methylmethacrylate bead placement where resection was not possible. When surgery was elected, massive amounts of fibrous adhesions within the abdomen were universally encountered.

Challenges to treatment included poor compliance with drug administration, adhesion formation impairing surgical access and identification of organs, manipulation/self-mutilation of surgical wounds on recovery, recrudescence of disease, concurrent disease, and misdiagnosis. Adverse sequelae to therapy included severe adhesion formation, intestinal torsion, peritonitis, dehiscence of incisions, inability to control additional abscess formation, and sepsis.

Outcome

Seven of 21 animals succumbed to sequelae of intra-abdominal abscessation. Two animals died of unrelated causes with no evidence of abscesses noted on necropsy. Ten animals survived the abscesses; of these, one is currently under treatment while the others appear resolved. Outcomes for two animals are unknown because of incomplete records. Two additional animals were diagnosed with abscesses in the latter part of 2002 and early 2003. To the author's knowledge these animals are currently stable.

Discussion

Preliminary findings suggest that intra-abdominal abscesses are an important problem in captive western lowland gorillas and are most likely to occur in older, obese, females. Affected females are usually reproductively quiescent, although a cause/effect relationship cannot be made at this time. One report on four senescent female gorillas describes cause of infertility as secondary to fibrous peritoneal adhesions attributed to endometriosis, possible pelvic inflammatory disease, and nonspecific trauma.¹³

Because strong similarities exist between great ape and human diseases,^14,17,19 advanced human diagnostic and treatment regimes can be explored for veterinary application. As additional normal animals added to the database for comparison of clinical signs, valuable guidelines can be suggested for identifying animals with possible abscesses. It appears that early diagnosis and intervention can result in a positive outcome. Further analysis is needed to determine the most successful treatments.

Limitations of this study include incomplete records, a lack of dietary information in records provided, an inability to compare diseased animals to the total captive animal population due to a low number of records, as well as an inability to compare the information with data from wild populations.

As data are compiled and completed, this ongoing project should continue to give pertinent information for identification and medical management of intra-abdominal abscesses in gorillas. Further, this database will serve as a useful tool for examining other disease issues within the population entered into the database.

ACKNOWLEDGMENTS

Drs. Robyn Barbiers and Tom Meehan made starting this project possible and I would like to extend my deepest thanks to them for ideas, input and support. Very special thanks to all the zoos that have contributed to this project: Audubon Park and Zoological Garden, Brookfield Zoo, Buffalo Zoological Gardens, Calgary Zoo, Cleveland Metroparks Zoo, Cheyenne Mountain Zoo, Cincinnati Zoo, Columbus Zoological Gardens, Dallas Zoo, Denver Zoological Gardens, Detroit Zoological Park, Gladys Porter Zoo, Grandby Zoo, Jacksonville Zoo, Knoxville Zoological Gardens, Lincoln Park Zoo, Little Rock Zoo, Miami Metro Zoo, Memphis Zoological Garden and Aquarium, Milwaukee County Zoological Gardens, North Carolina Zoological Park, Oklahoma City Zoological Park, Omaha's Henry Doorly Zoo, Pittsburgh Zoo, Rio Grande Zoo, San Diego Wild Animal Park, Santa Barbara Zoological Gardens, St. Louis Zoological Park, St. Paul's Como Zoo, Toledo Zoological Gardens, Topeka Zoo, Toronto Zoo, Utah's Hogle Zoo, Zoo Atlanta, and Zoo New England; apologies if any institutions are neglected mention here. I would also like to offer my never-ending gratitude to research assistants, Ellen Filurin and Kim Raymond who are diligently entering data into the gorilla medical database. Thanks to Dominic Travis, DVM and Ann Manharth, DVM for editorial input. Finally, I am indebted to Kevin Maxson for creating the database for this project.

Literature Cited

1.  Beregi A., S. Zorn, V. Molnar, and F. Biro. 2000. Ultrasonographic detection of abdominal abscess in two guinea pigs. Acta. Vet. Hung. 48(3):271–276.

2.  Braun U., U. Iselin, C. Lischer, E. Fluri. 1998. Ultrasonographic findings in five cows before and after treatment of reticular abscesses. Vet. Rec. 142(8):184–189.

3.  Bresnahan, J.F., U.G. Whitworth, Y. Hayes, E. Summers, and J.J. Pollock. 1984. Yersinia enterocolitica infection in breeding colonies of ruffed lemurs. J. Am. Vet. Med. Assoc. 185(11):1354–1356.

4.  Cousins, D. 1983. Mortality factors in captive gorillas. International Zoo News. 179(30):5–17.

5.  Cousins, D. 1972. Diseases and injuries in wild and captive gorillas. International Zoo Yearbook. 12:211–218.

6.  Goltenboth, R. 1982. Special section: diseases of zoo animals, non-human primates. In: Handbook of Zoo Medicine. Heniz-Geor, K (ed). Van Nostrand Reinhold Company, New York, NY. Pp: 46–85.

7.  Janssen, D.L. and R.M. Bush. 1990. Review of medical literature of great apes in the 1980s. Zoo Biol. 9:123–134.

8.  Janssen, D.L. 1993. Diseases of great apes. In: Zoo and Wild Animal Medicine. Fowler, ME (ed). W.B. Saunders Co, Philadelphia, PA. Pp: 334–340.

9.  Lambeth R.R., A.J. Dart, L. Vogelnest, C.M. Dart, D.R. Hodgson. 1998. Surgical management of an abdominal abscess in a Malayan tapir. Aust. Vet. J. 76(10):664–666.

10.  Mariadason, J.M., A. Catto-Smith, and P.R. Gibson. 1999. Modulation of distal colonic epithelia barrier function by dietary fiber in normal rats. Gut. 44(3): 394–399.

11.  McClean, K.L., G.J. Sheehan, and G.K.M. Harding. 1994. Intra-abdominal infections: a review. Clinical Infectious Diseases. 19:100–116.

12.  Meehan, T.P. and L.J. Lowenstine. 1994. Causes of mortality in captive lowland gorillas: a survey of the SSP population. Proc. Am. Assoc. Zoo Vet. Pp. 216–218.

13.  Munson, L. and R.J. Montalli. 1990. Pathology and diseases of great apes at the National Zoological Park. Zoo Biol. 9:99–105.

14.  Nizeyi J.B., R.B. Innocent, J. Erume, G.R. Kalema, M.R. Cranfield, T.K. Graczyk. 2001. Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda. J Wildl Dis. 37(2):239–244.

15.  Rumbaugh G.E., B.P. Smith, G.P. Carlson. 1978. Internal abdominal abscesses in the horse: study of 25 cases. J. Am. Vet. Med. Assoc. 172(3):304–309.

16.  Saber, A.A. and R.D. LaRaja. 2001. Abdominal Abscess. e-medicine, December 11, 2002: www.emedicine.com/MED/topic2702.htm, accessed April 18, 2003.

17.  Scott, G.B., and I.F. Keymer. 1975. Ulcerative colitis in apes: a comparison with the human disease. J Pathol. 115(4):241–244.

18.  Swenson, R.B. 1993. Protozoal parasites of great apes. In: Zoo and Wild Animal Medicine. Fowler, ME (ed). W.B. Saunders Co, Philadelphia, PA. Pp: 352–355.

19.  Urvater J.A., H. Hickman, J.L. Dzuris, K. Prilliman, T.M. Allen, K.J. Schwartz, D. Lorentzen, C. Shufflebotham, E.J. Collins, D.L. Neiffer, B. Raphael, W. Hildebrand, A. Sette, D.I. Watkins. 2001. Gorillas with spondyloarthropathies express an MHC class I molecule with only limited sequence similarity to HLA-B27 that binds peptides with arginine at P2. J. Immunol. 166(5):3334–3344.