Glomerular Atherosclerosis and Nephrosclerosis in Howler Monkeys
American Association of Zoo Veterinarians Conference 2003
Michael M. Garner1, DVM, DACVP; Janna E. Wynne2, DVM; Roberto F. Aguilar3, DVM; James T. Raymond1, DVM, DACVP; Linda J. Lowenstine4, DVM, PhD, DACVP; Robert W. Nordhausen5, MS
1Northwest ZooPath, Snohomish, WA, USA; 2The Los Angeles Zoo, Los Angeles, CA, USA; 3The Audubon Nature Institute, New Orleans, LA, USA; 4Pathology Service, Veterinary Medical Teaching Hospital, University of California, Davis, CA, USA; 5California Animal Health and Food Safety Laboratory, University of California, Davis, CA, USA

Abstract

Atherosclerosis and nephrosclerosis have been described in captive and wild howlers.5,7 This report describes the occurrence of glomerular atherosclerosis and nephrosclerosis in five black howlers (Alouatta caraya), three red howlers (Alouatta seniculus sara) and one golden howler (Alouatta seniculus straminea) from two zoological facilities in the United States. Table 1 summarizes the signalment and history for each animal. Two were males and seven were females. Age at necropsy ranged from 5–26 years, and average age was 16.1 years. Five animals died and four were humanely euthanatized. The most common reported historic findings included chronic renal failure (three animals), protein-losing nephropathy (two animals), weight loss (three animals), depression or lethargy (three animals) and constipation (two animals). Serum chemistries were available for seven monkeys and abnormal values included azotemia (seven animals), elevated serum creatinine (seven animals), hypoalbuminemia(seven animals), hypoproteinemia (six animals), hypercholesterolemia (five animals), and hyperphosphatemia (five animals). Urinalyses were available for four monkeys and abnormal values included proteinuria (three animals), hematuria (three animals), and glucosuria (three animals).

Table 1. Signalment and history for howler monkeys with glomerular disease

Case

Species

Age
(year)

Sexa

Clinical presentation

Blood chemistry values

Urinalysis

Disposition

1

Black

11

M

Protein-losing nephropathy

Azotemia
Hyperphosphatemia
Elevated creatinine
Hypercholesterolemia
Hypoproteinemia
Hypoalbuminemia

Proteinuria
Hematuria (trace)

Euthanatized

2

Black

19

F

Protein-losing nephropathy
Weight loss
Vomiting

Azotemia
Hyperphosphatemia
Elevated creatinine
Hypercholesterolemia
Hypoproteinemia
Hypoalbuminemia
Hyperglycemiab

Proteinuria
Hematuria (trace)
Glucosuriab

Died

3

Golden

18

F

Chronic renal failure
Weight loss
Constipation
Pica

Azotemia
Hyperphosphatemia
Elevated creatinine
Hypercholesterolemia
Hypoproteinemia
Hypoalbuminemia

Proteinuria
Glucosuria

Died

4

Red

5

F

Found recumbent and hypothermic

NAc

NA

Died

5

Red

16

F

Hospitalized for intensive care
No further history

Azotemia
Hyperphosphatemia
Elevated creatinine
Hypercholesterolemia
Hypoproteinemia
Hypoalbuminemia

NA

Died

6

Black

19

F

Lethargy and pulmonary congestion
Cardiomegaly

Azotemia
Hyperphosphatemia
Elevated creatinine
Hypoalbuminemia
Neutrophilic leukocytosis w/left shift
Mild anemia

NA

Euthanatized

7

Red

9

F

No history

Azotemia
Elevated creatinine
Hypoproteinemia
Hypoalbuminemia
Hypercholesterolemia
Regenerative anemia

NA

Died

8

Black

22

F

Lethargy
Emaciation
Kyphosis
Anemia
Chronic renal failure

Azotemiad
Elevated creatinine
Hypoproteinemia
Hypoalbuminemia
Mild anemia

Hematuria

Euthanatized

9

Black

26

M

Anorexia
Depression
Constipation
Kyphosis
Spondylosis
Chronic renal failure

NA

Hematuria
Proteinuria

Euthanatized

aM=male; F=female.
bAnimal was on fluid therapy at time urinalysis was obtained.
cNot available.
dMost recent bloodwork was 5 months prior to death.

Table 2 summarizes the gross and histologic findings for each animal. The most common gross findings were small, shrunken or scarred kidneys (seven animals), globoid or hypertrophic heart (four animals), thoracic or pleural effusions (four animals), aortic or valvular plaques (two animals), endocardiosis (two animals) and yellow fat (two animals). Histologically, all animals had varying and generally severe glomerular and renal vascular atherosclerosis, membranoproliferative and mesangioproliferative glomerulopathy, renal tubular protein casts, nephrosclerosis, and chronic interstitial nephritis. Extra-renal arteriosclerosis and atherosclerosis were detected in seven animals, especially in the heart and aorta. Eight animals had varying degrees of myocardial fibrosis. Some additional histologic findings included chronic enteritis or enterocolitis (six animals), pancreatic acinar cell atrophy (four animals), hemosiderosis in lymph nodes gut or liver (three animals), atrophy of fat (three animals), islet cell hyperplasia (two animals), and hyperplastic goiter (two animals).

Table 2. Gross and histologic lesions associated with glomerular disease in howler monkeys

Case

Gross findings

Renal histologic lesions

Other histologic lesions

1

Small kidneys
Yellow fat
Thick left ventricle

Atherosclerosis
MPGa
Sclerosis CINb
Protein casts

Goiter
Atrophy of fat
Pancreatic fibrosis and atrophy
Arteriosclerosis/atherosclerosis (heart valve)
Chronic colitis

2

Pale granular kidneys
Plaque on pulmonary valve

Atherosclerosis
MPG
Sclerosis
CIN

Goiter
Myocardial fibrosis
Hemosiderosis
Arteriosclerosis/atherosclerosis (ovary, vagina, aorta, kidney)
Pheochromocytoma
Chronic colitis

3

Small pale kidneys
Globoid heart with thick left ventricle
Thickened uterus

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Mycobacteriosis
Hemosiderosis
Myocardial fibrosis
Atherosclerosis/arteriosclerosis (heart)
Chronic colitis

4

Small pale pitted kidneys
Hypertrophic left ventricle

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Myocardial fibrosis
Myocardial infarction
Pancreatic acinar degeneration and fibrosis
Thyroid hypoplasia and fatty infiltration
Chronic enterocolitis

5

Generalized edema
Ascites
Hydrothorax
Diarrhea
Scarred kidneys

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Atherosclerosis (heart, stomach)
Myocardial fibrosis
Islet hyperplasia
Atrophy of fat
Chronic enteritis

6

Obesity
Pulmonary consolidation
Enlarged left atrium
Ascites
Hydrothorax

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Florid pulmonary edema
Myocardial fibrosis
Pancreatic acinar atrophy

7

Thin pale mucous membranes
Yellow fat
Hydrothorax
Aortic aneurism
Left ventricular hypertrophy
Endocardiosis

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Atherosclerosis/arteriosclerosis (aorta, spleen, urinary bladder, uterus, ovary, colon, pancreas)
Aortic aneurism
Myocardial fibrosis

8

Emaciation
Endocardiosis
Aortic plaques
Gastric ulcers
Pale foci in kidneys

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Atherosclerosis (mesentery, lymph node, spleen, aorta, ovary)
Myocardial fibrosis
Endocardiosis and arteriosclerosis
Gastric mineralization
Atrophy of fat
Acinar atrophy and islet hyperplasia

9

Ascites
Saponified fat
Small pale kidneys
Constipation

Atherosclerosis
MPG
Sclerosis
CIN
Protein casts

Atherosclerosis/arteriosclerosis (heart, spleen, intestine)
Chronic enteritis myocardial fibrosis
Hemosiderosis

aMembranoproliferative glomerulonephritis.
bChronic interstitial nephritis.

The renal lesions in these howlers were attributed to atherosclerosis, hypertension, ischemia, and aging. Glomerular protein leakage and tubular protein casts were attributed to glomerular atherosclerosis and glomerulosclerosis. The nephrosclerosis and chronic interstitial nephritis were attributed to tubular abrogation associated with protein casts as well as ischemic change associated with hypertension and atherosclerosis. The presentations in these animals are similar to various nephropathies described in humans that are associated with acquired derangements in lipid metabolism, atherosclerosis, diabetes mellitus, and hypertension.2-4,8-10 High circulating levels of low-density lipoproteins, glomerular-free radical injury, and ischemia are believed to play important roles in the development of chronic renal disease in humans.2-4,8-10 Chronic renal disease with protein losing nephropathy and atherosclerosis appear to be over-represented in captive howler monkeys fed diets that may not be considered atherogenic in other species, indicating that these animals may be exquisitely sensitive to the affects of hypercholesterolemia, atherosclerosis, and associated development of renal disease.1,5-7,11 Strict dietary management and periodic monitoring of serum cholesterol levels may be indicated for howler monkeys.

Literature Cited

1.  Chamberlain, J., G. Nelson, K. Milton. 1993. Fatty acid profiles of major food sources of howler monkeys (Alouatta palliata) in the neotropics. Experientia. 15:820–24.

2.  Galle, J., K. Heermeier. 1999. Atherogenic lipoproteins, oxidative stress, and cell death. Kidney Int. Suppl. 71:S62–65.

3.  Gin, H., V. Rigalleau, M. Aparicio. 2000. Lipids, protein intake, and diabetic nephropathy. Diabetes Metab. 4:45–53.

4.  Makanjuola, A.D., M. Suresh, P. Laboi, P.A. Kalra, J.E. Scoble. 1999. Proteinuria in atherosclerotic renovascular disease. QJM. 92: 515–18.

5.  Malinow, M.R., C.A. Maruffo. 1965. Aortic atherosclerosis in free-ranging howler monkeys (Alouatta caraya). Nature. 206:948–949.

6.  Malinow, M.R., C.A. Maruffo. 1966. Naturally occurring atherosclerosis in howler monkeys (Alouatta caraya). J. Atheroscler. Res. 6:368–380.

7.  Malinow M.R., C.A. Storvick. 1968. Spontaneous coronary lesions in howler monkeys (Alouatta caraya). J. Atheroscler. Res. 8:421–431.

8.  Moorhead J.F., C. Brunton, R.L. Femando, A. Bums, Z. Varghese. 1996. Do glomerular atherosclerosis and lipid­mediated tubulo-interstitial disease cause progressive renal failure in man? Blood Purif. 14:58–66.

9.  Moorhead, J.F., C. Brunton, Z. Varghese. 1997. Glomerular atherosclerosis. Miner Electrolyte Metab. 23:2387–90.

10.  Rodriguez-Porcel, M., J.D. Krier, A. Lerman, P.F. Sheedy, J.C. Romero, C. Napoli, L.O. Lerman. 2001. Combination of hypercholesterolemia and hypertension augments renal function abnormalities. Hypertension. 37:774–80.

11.  Vie, J.C., B. Moreau, B. de Thoisy, P. Fournier, C. Gentry. 1998. Hematology and serum biochemistry values of free-ranging red howler monkeys (Alouatta seniculus) from French Guiana. J. Zoo Wildl. Med. 29:142–149.

 

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

Michael M. Garner, DVM, DACVP
Northwest ZooPath
Snohomish, WA, USA


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