Evaluation of Blood Lipid Profiles as Part of a Complete Cardiac Assessment in Western Lowland Gorillas (Gorilla gorilla gorilla)
American Association of Zoo Veterinarians Conference 2003

Eric J. Baitchman1, DVM; Mark H. Goldberger2, MD, FACC; Michele Nanna3, MD, FACC; Paul P. Calle1, VMD, DACZM; Tracy L. Clippinger1,4, DVM, DACZM; Sharon L. Deem1,5, DVM, PhD, DACZM; Stephanie B. James1, DVM, DACZM; Bonnie L. Raphael1, DVM, DACZM; Robert A. Cook1, VMD

1Department of Clinical Care, Wildlife Health Sciences, Wildlife Conservation Society, Bronx, NY, USA; 2North Central Bronx Hospital, Bronx, NY, USA; 3Cardiac Care and Vascular Medicine, PLLC, Bronx, NY, USA; 4Present address: Zoological Society of San Diego, San Diego, CA, USA; 5Present address: National Zoological Park, Smithsonian Institute, Washington, D.C., USA

Abstract

As much as 41% of mortality in captive, adult lowland gorillas has been attributed to cardiovascular disease.12 Hypercholesterolemia has been considered a likely etiologic factor in the development of heart disease in gorillas,8,15 but the definition of what constitutes hypercholesterolemia in this species is uncertain1,6,11. In humans, treatment is recommended for cholesterol levels greater than 200 mg/dl.13 The average cholesterol level in gorillas, however, is over 280 mg/dl.5,11 In human patients, hypercholesterolemia is an important factor in the development of atherosclerosis and subsequent coronary heart disease, with the most common clinical sequelae being myocardial and cerebral infarction.3,9,14 Atherosclerosis in gorillas has been reported with some frequency,4,8,15,17 but has only rarely been directly associated with mortality.4,15. Furthermore, the incidence of atherosclerosis in gorillas has not previously been correlated with hypercholesterolemia.1 This study describes lipid profile results and proposes a possible correlation between specific lipid levels and risk of atherosclerosis in gorillas.

Fifteen gorillas (five males and ten females), ranging in age from 3–40 yr, were evaluated by blood lipid profile and transesophageal echocardiography. The lipid profile included total cholesterol, high-density lipoprotein (HDL), cholesterol/HDL (Chol/HDL) ratio, low-density lipoprotein (LDL), apolipoprotein B (Apo B), apolipoprotein A1 (Apo A1), apolipoprotein B/A1 ratio, and triglyceride. Transesophageal echocardiography (Hewlett-Packard Sonos 1000, 5 MHz transesophageal probe, Hewlett-Packard, Melville, NY, USA) was performed only on animals greater than 5 yr, including two males (30 and 40 yr old) and eight females (9–36 yr old).

Transesophageal echocardiography demonstrated five animals with atherosclerotic plaques in the descending aorta. One 40-yr-old male was found to have a grade II atheroma, and four females, aged 10, 26, 27, and 36 yr, had grade I atheromas (based on published grading system).7 Animals were identified as "affected" or "unaffected" based on presence of plaques. For the purposes of statistical analysis, the five youngest animals that were not examined with echocardiography are included in the "unaffected" group. It is extremely unlikely that these juveniles would have atheromas.

Average total cholesterol for this population was 261.9±64.5 (n=15). This is consistent with previously reported cholesterol values for gorillas (284±83, n=863).5 For all animals, there was a negative correlation of HDL levels with age (Pearson product moment correlation, -0.72, p=0.002). There was a positive correlation of both Chol/HDL (0.72, p=0.002) and Apo B/A1 (0.69, p=0.004) with age. There were significant differences in age (unpaired t-test, p=0.007), Chol/HDL ratios (Mann-Whitney rank sum test, p=0.023), and Apo B/A1 ratios (Mann-Whitney rank sum test, p=0.027) between affected and unaffected groups. No significant correlations were found for LDL or triglycerides with age nor were there significant differences between affected and unaffected groups for total cholesterol or any other individually measured lipid (significance defined at p<0.05).

In human patients, evaluations of lipid profiles are useful in predicting risk of coronary heart disease.2,10,13,18 Thus, it might follow that lipid profiles are also useful in predicting risk of disease in gorillas. In this study, using atherosclerosis as an indicator of the presence of coronary heart disease, elevated ratios of Apo B/A1 and Chol/HDL, were the most significant. This is consistent with what is reported in human literature.2,10,18 HDL is considered protective against atherogenesis.13 HDL transports cholesterol out of cells and may also inhibit oxidation and accumulation of LDL, which transports lipids into cells and promotes atherogenesis and thrombus formation. Indeed, low HDL is itself a strong independent predictor of coronary heart disease in humans.2,13 In this group of gorillas, as age increased, HDL decreased without significant concomitant change of LDL. The resultant increase of Chol/HDL ratio appears to contribute to development of atherosclerosis. Apolipoproteins are components of the lipoproteins, with Apo A1 associated with HDL and Apo B associated with LDL. As their relationships suggest, Apo A1 is considered protective and Apo B is considered to contribute to risk.

This study suggests that evaluation of complete lipid profiles as part of a comprehensive cardiac evaluation in gorillas may be valuable. It is misleading to evaluate total cholesterol alone as an indicator of coronary health. There was no significant difference in total cholesterol between the affected and unaffected groups. The findings reported here may imply a relationship between specific lipid ratios and possible correlation to risk of coronary disease. As more data become available from a greater number of animals, these conclusions may be challenged. It is the hope of the authors that this study be used as a starting point to increase the database of measured lipid profiles and to increase understanding of hypercholesterolemia in gorillas.

Acknowledgments

Dr. John Wehr, Fordham University, Bronx, New York, provided invaluable assistance with statistics.

Literature Cited

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2.  Frick, M.H., V. Manninen, J.K. Huttunen, O.P. Heinonen, L. Tenkanen, and M. Manttari. 1990. HDL-Cholesterol as a risk factor in coronary heart disease—an update of the Helsinki Heart Study. Drugs. 40, Suppl. 1:7–12.

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5.  International Species Information System. 2001. Physiological Reference Values for Gorilla gorilla gorilla. International Species Information System. Apple Valley, Minnesota.

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8.  Kenny, D.E., R.C. Cambre, T.P. Alvarado, A.W. Prowten, A.F. Allchurch, S.K. Marks, and J.R. Zuba. 1994. Aortic dissection: an important cardiovascular disease in captive gorillas. J. Zoo Wildl. Med. 25:561–568.

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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.  National Cholesterol Education Program. 2002. Third Report of the National Cholesterol Education Program Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). National Institutes of Health. NIH Publication No. 02-5215.

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15.  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. 26:43–51.

16.  Scott, N.A., R. McManamon, E. Strobert, G.D. Cipolla, N. Tarazona, and R.B. Swenson. 1995. In vivo diagnosis of coronary artery disease in a western lowland gorilla. J. Zoo Wildl. Med. 26:139–143.

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Speaker Information
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Eric J. Baitchman, DVM
Department of Clinical Care
Wildlife Health Sciences
Wildlife Conservation Society
Bronx, NY, USA


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