Abstract

An adult female California sea lion (Zalophus californianus) presented to the Aquarium of the Pacific with a six-month history of persistent bilateral mucoid nasal discharge. Two years previously, this sea lion of unknown age (presumed geriatric) was found stranded in San Diego, California and was rehabilitated by Sea World of California for five months. During rehabilitation, she gained a total of 29.5 kg but was deemed un-releasable due to poor vision and suspected limited survivability in the wild.

In May 1998, the sea lion became part of the collection at the Aquarium of the Pacific, which consisted of one adult male and two juvenile female California sea lions and three adult female harbor seals (Phoca vitulina) housed in an outdoor, 953,800 L (251,000 gal), natural seawater exhibit pool. Although the sea lion maintained her weight and ate on her own, she developed a stereotypy within 5 months of being placed on exhibit. This behavior consisted of positioning herself vertically in a far comer of the exhibit with her hind flippers at the surface and moving her head in a circular motion for 30-60 sec at a time before taking a breath and returning to her stereotypical movements. Furthermore, handlers found it challenging to train her for any complex behaviors.

In January 2000, the sea lion had developed generalized, ventral flipper erosions and ulcerations, presumed to be due to trauma from non-slip, granular surfaces surrounding the exhibit pool. In February 2000, the ulcers began bleeding superficially at regular intervals and the sea lion was separated for observations and treatments into a 30,400 L (8,000 gal) round holding pool surrounded by smooth wooden decks. In May 2000, she developed a mucoid, tan to greenish nasal discharge that was intermittently bilateral and prevented effective nasal breathing, forcing the sea lion to adapt to breathing exclusively through her mouth. Because the holding pool was shallow, the cycle of stereotypical head movements subsided.

Various treatments, including antibiotics, anti-histamines, and steroids, were tried for two years at different times, but no improvements in flipper lesions or degree of nasal discharge were apparent.

In September 2000, a team of veterinarians, technicians, staff, and volunteers performed a series of procedures on the sea lion consisting of anesthesia, physical examination, oral/dental exploration, complete blood count, serum chemistries, urinalysis, fecal culture and Baermann test, nasal discharge cultures, rhinoscopy (with biopsies), gastroscopy, head radiographs, abdominal ultrasound, and flipper biopsies.

For these procedures, the sea lion was restrained by squeeze cage and immobilized using a combination of medetomidine (11 mcg/kg), midazolam (0.2 mg/kg), and butorphanol (0.25 mg/kg) given i.m. at the same time (in separate syringes). At 30 min following initial injections, a facemask was placed over her nose and mouth to deliver isoflurane, and atropine was given i.m. (0.02 mg/kg). She was intubated and maintained on 1 - 2.5% isoflurane for 75 min with excellent results. Isoflurane was tapered and discontinued 10 min prior to completing procedures. Anesthesia was reversed using atipamezole (55 mcg/kg), flumazenil (11 mcg/kg), and naltrexone (0.13 mg/kg) all i.m. and 100% oxygen was delivered via endotracheal tube until extubation at 9 min post-reversal. The sea lion was monitored in a squeeze cage until she appeared fully awake at 60 min post-reversal and could be released to her pool.

Abnormal physical exam findings included: halitosis with food debris clinging to the palate and teeth, bilateral mature cataracts, generalized bilateral ventral flipper erosions and ulcerations, and copious mucoid nasal discharge. Significant clinical pathology findings included: non-regenerative anemia, leukocytopenia, elevated CK, and low progesterone. Heartworm and cryptococcus antigen tests were negative.

Gastric mucosa was normal based on gastroscopy, and ultrasound images of kidneys, urinary bladder, liver, and spleen were normal. Flipper lesions were classified as chronic ulcerative inflammation with no evidence of infectious organisms. Cytology of nasal exudate from the outer nares showed suppurative exudate with intralesional bacteria.

Head radiographs appeared within normal limits. Rhinoscopy revealed a smooth, mucosa-lined structure completely obstructing the rostral nasopharyngeal region at the junction of the soft and hard palates. The obstruction was firm and multiple attempts to obtain biopsies through the endoscope were not successful. Biopsies of two polypoid, 3-5 mm pink nodules visualized on the floor of the rostral nasal cavity were characterized as chronic/suppurative inflammation and granulation tissue.

Over the next two months, treatment included non-steroidal anti-inflammatories, broad-spectrum antibiotics and de-wormers, iron with folic acid, and B complex vitamins. The nasal discharge and flipper lesions persisted as before with little improvement.

In November 2000, the sea lion was anesthetized for a spiral computed tomography (CT) scan of her head and thorax at a local hospital, involving significant media attention and extensive pre- procedural planning. Rhinoscopy, flipper biopsies, and blood work were repeated at the same time.

The CT scan showed a 3-4 mm thick membranous structure spanning the region between the soft and hard palates, a mildly deviated nasal septum, and collections of discharge throughout the nasal turbinates. Cranial bony structures and the lower respiratory tract otherwise appeared within normal limits. The obstructive membrane was visualized using rhinoscopy and, unlike the first examination, could be penetrated with a biopsy instrument for multiple samples and cultures.

Bloodwork confirmed continued non-regenerative anemia (reticulocyte production index of 0). Serum iron and total iron binding capacity levels were 49 and 166 mcg/dl, respectively. Cultures of the obstructive nasopharyngeal tissue, nasal exudate (taken from deep into the turbinates), and exudate lining the interior of the endotracheal tube primarily grew Pseudomonas aeruginosa. Repeat flipper biopsies showed chronic ulcerative dermatitis and melanin incontinence, possibly trauma-induced. Biopsies of the obstructive nasopharyngeal membrane revealed ulcerated granulation tissue with suppurative inflammation. One biopsy contained a section of a large, partially disintegrated parasite.

Following a preliminary diagnosis of verminous and bacterial rhinitis, the sea lion received broad-spectrum antibiotics, de-wormers (in case of any persistent, live nasal parasites), steroids, vitamins (B complex, C), nutraceuticals (for possible arthritic limbs), and topical therapies for flipper ulcers. Treatments resulted in minimal clinical improvement overall; however, a course of prednisone (0.25 mg/kg p.o. twice daily for 7 d, once daily for 7 d, then every other day for 7 doses) appeared to have a positive effect on appetite and attitude.

Review of the nasal tissue biopsies by a parasitologist (C. Gardiner) further characterized the parasite as a maggot with a thick cuticle and chitinized tubes consistent with tracheal rings (species not identifiable).

We hypothesize that before being rescued, the sea lion sustained a nasal infestation with maggots (nasal myiasis) that resulted in a persistent, bacterial, suppurative rhinitis after the maggots had died. The presence of chronic inflammation resulted in growth of a proliferative, obstructive nasopharyngeal membrane, continued bacterial colonization, and bilateral mucoid discharge. These lesions contribute to an inability to breathe nasally. The observed stereotypy may be a behavioral reaction to nasal pressure and discomfort from the blocked passages and nasal discharge, and/or cataracts and poor vision.

In an attempt to restore normal breathing patterns, treatments will include several surgical debridements of the abnormal retropharyngeal tissue using a carbon-dioxide laser, guided by a rigid rhinoscope. Surgery will be followed by daily nebulization with aminoglycosides and mucolytics, and oral anti-inflammatories. We also plan to surgically debride and topically treat flipper lesions, and to evaluate and possibly remove both cataracts. Our goals are to provide a higher quality of life for this geriatric, well-loved sea lion and to return her to the main exhibit.

Acknowledgements

We thank the dedicated curators, mammalogies, aquarists, life support, facilities, media relations staff, and volunteers at the Aquarium of the Pacific for their support during procedures and treatments. Special gratitude is extended to Dr. Lucy Spelman (Smithsonian National Zoological Park) for sea lion anesthetic protocols, to Dr. William Van Bonn (Navy Marine Mammal Program) and Keith Matassa (Marine Mammal Care Center in San Pedro, CA) for their valuable assistance during procedures, and to all the marine mammal veterinarians contributing consulting advice for this case. We acknowledge the St. Mary's hospital in Long Beach, especially the radiology staff, for their support and donation of a CT scan. We thank Roy Brown of Histology Consulting Service, Oak Harbor, WA, for histology support.