Abstract

Primary lipid keratopathy refers to lipid infiltration into the cornea that occurs in the absence of underlying ocular pathology and is associated with disorders of lipid metabolism. Lesions of primary lipid keratopathy consist of hazy or crystalline to dense white corneal opacities that occur initially at the limbus and advance towards the central cornea as the disease progresses.^1,2,4 Several cases of lipid keratopathy in anurans have been reported in the literature; however, the causes and risk factors associated with the disease in these species remain obscure.^3,5,6 The purpose of this study was to further identify susceptible species of amphibians and reptiles, and factors predisposing to the development of the disease. A survey of 28 North American zoos was conducted and retrospective and current cases at the Toronto Zoo were reviewed.

In the survey, fourteen zoos reported a total of 28 cases of lipid keratopathy in the following species of anurans: Litoria caerulea, Litoria aurea, Osteopilus septentrionalis, Agalychnis callidryas, Hyla arenicolor, Hyla eximia, Dyscophus antongilii, Kaloula pulehra, Ceratophrys ornata, Scaphiopus couchii and Bufo guttatus.

At the Toronto Zoo, all five adult female White’s tree frogs (Litoria caerulea) previously held in the collection had high serum cholesterol and developed lipid keratopathy, while three male conspecifics were unaffected and had low serum cholesterol (Table 1). The diet consisted of crickets three times weekly and pinkies once weekly. Currently, the zoo houses three females that are fed crickets three times weekly and pinkies once monthly and have low serum cholesterol (Table 1). One of these females has lipid keratopathy. Values from unaffected captive New Guinea tree frogs, fed crickets three times weekly and pinkies once weekly, are presented for comparison (Table 1).

Table 1. Serum cholesterol values and signalment of anurans at Toronto Zoo

^aValues are expressed in mmol/L. The value is presented as a mean (range) if the number of individuals sampled exceeded three. Otherwise, the values for each individual are separated by commas. Several of the means include multiple determinations at different times on individual frogs. 0.9 mmol/L is the limit of detection of the cholesterol assay.
^bUnless otherwise stated, a (+) or (–) indicates whether all animals in the group had, or did not have, lipid keratopathy.

Four out of five female Colorado river toads (Bufo alvarius) previously in the collection had lipid keratopathy. There are currently 6 females in the collection, two of which have lipid keratopathy. The diet has always consisted of crickets fed three times weekly and pinkies once weekly. Both affected and unaffected females have high mean serum cholesterol (Table 1). Serum cholesterol determinations repeated over several years revealed wide fluctuations within individuals. Serum cholesterol values for three female Marine toads (Bufo marinus), fed the same diet, are presented for comparison (Table 1).

The findings in this review of retrospective and current cases are consistent with the literature in that lipid keratopathy appears to be primarily a disease of older female frogs of certain species. The disease is more frequent in females that have high serum cholesterol. Although the literature suggests the feeding of pinkies as a cause,^3,6 some species fed pinkies maintain low serum cholesterol and are not predisposed to lipid keratopathy. As part of a larger study investigating the cause of lipid keratopathy in Cuban tree frogs, we have induced the disease in female frogs fed only crickets. In these animals, both female and male frogs developed elevated serum cholesterol in captivity, compared to wild conspecifics. Captive females affected with lipid keratopathy had significantly higher serum cholesterol values than unaffected captive females.

Lipid keratopathy in reptiles has not been described in the literature. In the survey, four plumed basilisks (Basilisk plumifrons), two speckled Cape tortoises (Homopus signatus) and one Madagascan day gecko (Phelsuma madagascariensis) were identified as having lipid keratopathy. At the Toronto Zoo, there have been two cases of primary lipid keratopathy in female plumed basilisks, and one in a female green water dragon (Physignathus cocincinus). Their diet consists of crickets three times weekly and pinkies and mealworms once weekly. The green water dragons are also fed mixed vegetables once weekly. Repeated cholesterol determinations on several animals in the collection revealed high serum cholesterol in most individuals of both sexes (Table 2). This appears to indicate that either high serum cholesterol is normal in both sexes of these species, or both sexes have problems with lipid metabolism in captivity. Because all basilisks and water dragons had high serum cholesterol, no association can be made with the presence of lipid keratopathy.

Table 2. Serum cholesterol values and signalment for reptiles at the Toronto Zoo.

^aValues are expressed in mmol/L. Most of the serum cholesterol values for individuals are averages of two or three determinations made in that individual over a period of years.
^bA (+) or (–) indicates whether all animals in the group had, or did not have, lipid keratopathy.

Acknowledgments

We thank the respondents of the lipid keratopathy survey. We also thank past Toronto Zoo resident Karrie Rose for historic serum cholesterol determinations. We are grateful to the keepers of the Toronto Zoo Animal Health Unit for assistance with the care and feeding of the Cuban tree frogs. The Toronto Zoo Foundation and Association of Reptile and Amphibian Veterinarians provided financial support. This work was completed as partial fulfillment of a Doctor of Veterinary Science graduate degree by the senior author.

Literature Cited

1.  Barchiesi BJ, Eckel RH, Ellis PP. The cornea and disorders of lipid metabolism. Surv Ophthal. 1991;36:1–22.

2.  Bron AJ. Corneal changes in the dislipoproteinemias. Cornea. 1989;8:135–140.

3.  Carpenter JL, Bacharach Jr. A, Albert DM, Vainsi SJ, Goldstein MA. Xanthomatous keratitis, disseminated xanthomatosis, and atherosclerosis in Cuban tree frogs. Vet Pathol. 1986;23:337–339.

4.  Crispin SM, Barnett KC. Dystrophy, degeneration and infiltration of the canine cornea. J Small Anim Pract. 1983;24:63–83.

5.  Dziezyc J, Millichamp NJ. Lipid keratopathy in frogs. In: Proceedings of the Third International Colloquium on Pathology of Reptiles and Amphibians; 1989:95–96.

6.  Russell WC, Edwards Jr. DL, Stair EL, Hubner DC. Corneal lipidosis, disseminated xanthomatosis, and hypercholesterolemia in Cuban tree frogs (Osteopilus septentrionalis). J Zoo Wildl Med. 1990;21:99–104.