Abstract

A long-term captive group of California sea lions (Zalophus californianus) was established at the San Diego Zoo (SDZ) in the early 1970s as part of an interactive display highlighting the abilities of various vertebrates for the education and entertainment of zoo visitors. As the group began to age, several age-related degenerative problems were being discovered in this otherwise healthy group of neutered males. One of these sea lions, a 28-year-old male, had a history of slowly progressive degenerative joint disease and bilaterally luxated cataracts and periodontitis. As part of a program of geriatric palliation, the sea lion was undergoing treatments with low dose oral butorphanol and/or ibuprofen PRN for ocular pain associated with the cataract luxations, and oral glycosaminoglycans as palliative therapy to relieve signs of progressing arthritis in several joints. Based on appetite, attitude, and willingness to perform learned behaviors, the animal appeared to be responding well to the palliative efforts.

In order to continue the interactive display the San Diego Zoo acquired a young wild sea lion that had been rescued from starvation by a regional marine mammal rescue center. After recovering at the rescue center, the young sea lion was transferred to the zoo and placed into quarantine at the zoo hospital. Quarantine lasted from 15 March 1999 to 12 April 1999. During its quarantine stay, the animal was weaned onto the SDZ diet, and trainers would come to the hospital as the last activity of the day to work with the young sea lion and acquaint him to his new trainers and his new routine. Daily body weights were obtained by training the animal to sit in a large kennel placed on a scale. Routine fecal analyses for parasites and bacterial pathogens yielded Campylobacter lari, which had also been observed as an incidental gut floral inhabitant in the long-term captives as well. On 8 April, the sea lion was observed to have a mild dermatitis in the skin along the ventral cervical midline that resolved without treatment. No medical testing to characterize the dermatitis was attempted, due to the self-limiting nature of the condition. The animal was bled for routine blood tests (CBC, serum chemistry panel), and serum was banked at -70°C. Aside from being sluggish to wean onto the SDZ diet, the young animal remained outwardly healthy through his quarantine evaluation, and was released to his own holding tank at the interactive display exhibit. He had access to the same deck that the older sea lion used, and was housed in the same water system, but did not come into direct physical contact with any of the other animals in the exhibit.

While in the process of establishing baseline limb radiographs for the older animal’s arthritic condition, keepers and registered veterinary technicians were working together to train it to voluntarily allow radiographs to be taken with a field radiograph unit. On 31 May 1999, while training the animal to sit on a radiograph cassette, keepers noted that it was refusing to use its rear flippers and appeared slightly depressed. A request for a veterinary evaluation was made. An examination under voluntary restraint revealed a swelling of the volar surface of the left rear flipper. With thermography, the area was visibly elevated in temperature, indicating the possibility of an inflammatory process. Over the next few days, the older animal became progressively more sluggish, preferred to haul himself out of the water, and began to refuse food. On 4 June 1999, the lesion on the left rear flipper had developed to a large vesicle and subsequently erupted when the animal moved around on the decking outside of his pool. The erupted vesicle revealed clean granulation tissue only. Closer inspection of front and rear flippers revealed that he was developing a multifocal vesicular dermatitis consistent with reported signs of caliciviral infection.¹

On 7 June the older animal was voluntarily restrained for a clinical evaluation of his condition. Blood was sampled from between the rear digits at the level of the metatarsal bones after infusing a small amount of lidocaine into the phlebotomy site. In addition, a mature vesicle was selected to aspirate. The site was prepared with three alcohol/chlorhexidine scrubs, and rinsed well with sterile, nonbacteriostatic lavage fluid to remove residual astringent. The vesicle was aspirated, yielding approximately 1 ml of yellowish, slightly turgid fluid which on cytology was consistent with an inflammatory exudate. No microorganisms were seen on smears of the aspirate. Bacterial culture yielded a variety of skin contaminants, despite rigorous attempts to disinfect the skin over the vesicle. A small aliquot of the sample was sent to Texas Veterinary Diagnostic Laboratory for transmission electron microscopy (TEM) to rule out a viral etiology. Another small aliquot of the sample was sent to the College of Veterinary Medicine, Laboratory for Calicivirus Studies, Oregon State University, Corvallis, OR 97331 USA. A calicivirus consistent with San Miguel Sea Lion Virus was isolated from the vesicular fluid. Serotyping of the isolate is pending.

The older animal’s condition continued to decline over the following week, despite supportive efforts. On 14 June 1999 it was euthanatized after a review of his advanced age and mounting medical problems revealed that his quality of life was rapidly deteriorating. At necropsy, multiple age-related degenerative problems were identified in addition to the ulcerative caliciviral skin infection.

In addition to acclimation and identification needs of new acquisitions, quarantine procedures are designed to minimize the exposure of an established population to novel or otherwise devastating infectious diseases. In this case, it was assumed that a 4-week quarantine period for an animal that had been isolated from wild sea lions for considerably longer than the SDZ quarantine period would suffice to ensure that no serious infectious diseases would be introduced into the long-term captives at SDZ. Given the circumstantial temporal evidence and the long-standing stable nature of the aging captive group, the young animal was chronically infected with, and shedding a calicivirus. In retrospect, it is possible for the mild dermatitis that was seen in quarantine to have been caliciviral in origin. To date, the effects of introducing calicivirus into the established group appears to have manifested problems only in the older animal, as the other animals have remained unaffected.

Diagnosis of caliciviral infection depends on identification of viral particles and associated lesions, as in this case. Viral serology is valuable for conducting epidemiologic surveys in contact animals and humans. Treatment of caliciviral infections currently relies on supportive care measures and prevention/treatment of secondary/opportunistic bacterial, fungal, and parasitic diseases. In this case we were fortunate to find viral particles on TEM of vesicular fluid, and to confirm the caliciviral nature of the vesicular skin disease with viral culture.

Concern over the zoonotic potential of caliciviruses associated with marine life is increasing.⁴ Caliciviruses are known to infect a broad range of hosts, including non-vertebrates.² In addition, caliciviral infections are considered to be among the leading causes of gastrointestinal viral infections in humans.³ A calicivirus associated with human illness isolated from a pinniped has been documented.⁴ Of perhaps greatest concern to some researchers in the field is the potential for severe, possibly life-threatening caliciviral infections, such as in pregnant women associated with the so-called hepatitis E virus (a calicivirus). Although this virus has not been associated with marine life to date, researchers caution that until more information is obtained about the origins, reservoirs, and distribution of caliciviruses the risk of mild to severe disease in humans associated with these viruses exists.

Literature Cited

1.  Gage LJ, Amaya-Sherman L, Roletto J, Bently S. Clinical signs of San Miguel sea lion virus in debilitated California sea lions. J Zoo Wild Med. 1990;21(1):79–83.

2.  Poet SE, Skilling DE, DeLong RL, Smith AW. Detection and isolation of a calicivirus from a bivalve mollusk (Mytilus californianus) collected from rocks adjacent to pinniped rookeries. In: Proc Intl Assoc Aquat Anim Med. 1994;25:106.

3.  Smith AW, Berry ES, Skilling DE, Barlough JE, Poet SE, Berke T, Mead J, Matson DO. In vitro isolation and characterization of a calicivirus causing a vesicular disease of the hands and feet. Clin Infect Dis. 1998;26(2):434–439.

4.  Smith AW, Skilling DE, Cherry N, Mead JH, Matson DO. Calicivirus emergence from ocean reservoirs: zoonotic and interspecies movements. Emerg Infect Dis. 1998;4(1):13–20.