Otostrongylus circumlitus Infestation and Disseminated Adenovirus Infection in a Stranded California Sea Lion (Zalophus californianus)
IAAAM Archive
Kathleen M. Colegrove1; Elizabeth L. Buckles1; Linda J. Lowenstine1; Terra Kelly2; Murry D. Dailey3; Martin Haulena3; Frances M.D. Gulland3
1Veterinary Medical Teaching Hospital and Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA, USA; 2Environmental Medicine Consortium and Department of Clinical Sciences, North Carolina State University, Raleigh, NC, USA; 3The Marine Mammal Center, Marin Headlands, Sausalito, CA, USA


Otostrongylus circumlitus is a metastrongyle nematode that is a well recognized cause of respiratory disease in phocid seals.6,7 Along the California coast O. circumlitus causes bronchitis and bronchiolitis in stranded Pacific harbor seals (Phoca vitulina richardsii), and arteritis, thrombosis, interstitial pneumonia, and disseminated intravascular coagulation (DIC) in stranded northern elephant seals (Mirounga angustirostris). In harbor seals adult nematodes are typically found within bronchi and bronchioles. In contrast, O. circumlitius nematodes in elephant seals are more often found in the right ventricle, pulmonary artery, and pulmonary arterioles. Lesions are often caused by immature nematodes. It has been suggested that the distribution and lesions associated with infection in elephant seals is due to recent host-parasite association and reaction to the parasites early in their migration.6 Verminous pneumonia in California sea lions (Zalophus californianus) is most commonly caused by Parafilaroides decorus.4 To our knowledge there have been no reports of O. circumlitus infection in otariids. There are two reports of adenovirus infection in California sea lions, documenting six affected animals. All six sea lions had acute necrotizing hepatitis associated with adenoviral nuclear inclusions.1,3

An approximately one-year-old, male California sea lion stranded and was admitted to The Marine Mammal Center, Sausalito, CA. On initial physical exam the animal was emaciated and had mild diarrhea. Hematology results at admission included mild leukocytosis and neutrophilia. Two weeks following admission, the animal became anorexic and blood and mucous were observed coming from the oral cavity. Corneal opacity was observed in the right eye. Hematology results included leukocytosis consisting of a neutrophilia with a left shift, anemia, and thrombocytopenia. The animal died two days later. On post mortem examination, two large nematodes were observed in the right ventricle of the heart, and approximately 150 similar appearing worms were observed in the pulmonary artery and arterioles. Multiple areas of hemorrhage were scattered throughout all lung lobes, and on cut section blood vessels were occluded by fibrin thrombi. No parasitic ova or larvae were observed on a fecal sample obtained at necropsy. Aerobic culture of the lung yielded a pure growth of E. coli. Nematodes collected from the pulmonary artery at necropsy were identified via morphologic characteristics as immature forms of O. circumlitus.7

Histologic findings in the lungs included severe suppurative and necrotizing arteritis with vascular thrombosis, interstitial pneumonia, and large areas of pulmonary hemorrhage. Cross sections of large nematodes were often found within affected arteries and within fibrin thrombi. Lesions were similar to those found in northern elephant seals with O. circumlitus infection.6 The hilar lymph node was enlarged and contained multiple areas of hemorrhage. Lesions in the right eye included ulcerative keratitis, corneal edema, and mild conjunctivitis. Large, amphophilic intranuclear inclusions were noted in endothelial cells throughout the lung, hilar lymph node, spleen, cornea, iris, and conjunctival epithelium. Inclusions were not discerned in the liver.

Ultrastructural examination of the hilar lymph node using transmission electron microscopy revealed scattered viral particles within the nucleus of endothelial cells. Virons were nonenveloped, hexagonal, and averaged 70 µm in diameter. These morphologic features are characteristic for adenoviruses.2 Immuohistochemical stains against bovine adenovirus-5 were completed on sections of lung and hilar lymph node. Moderate numbers of intranuclear viral inclusions were noted in endothelial cells using this technique. Serologic titers were negative for canine adenovirus-1 on serum collected at the time of necropsy.

The relationship between these two pathogens in this sea lion is uncertain at this time. Poor nutritional condition may have resulted in increased susceptibility to both parasitic disease and viral infection.5 Alternatively, viral recrudescence may have occurred secondary to severe parasitic disease. PCR analysis is currently being completed to further characterize the virus and its possible relatedness to other mammalian adenoviruses.


The authors wish to thank the staff and volunteers of The Marine Mammal Center and Bob Nordhausen for electron microscopy.


1.  Britt JO, AZ Nagy, EB Howard. 1979. Acute viral hepatitis in California sea lions. Journal of the American Veterinary Medical Association 175(9):921-923.

2.  Cheville NF. 1994. Ultrastructural Pathology, An introduction to interpretation. Iowa State University Press, Ames, Iowa. Pp. 514-517.

3.  Dierauf LA, LJ Lowenstine, C Jerome. 1981. Viral hepatitis (Adenovirus) in a California sea lion. Journal of the American Veterinary Medical Association 179(11):1194-1197.

4.  Gerber JA, J Roletto, LE Morgan, DM Smith, LJ Gage. 1993. Findings in pinnipeds stranded along the central California coast, 1984-1990. Journal of Wildlife Diseases 29(3):423-433.

5.  Gershwin ME, AT Borchers, CL Keen. 2000. Phenotypic and functional considerations in the evaluation of immunity in nutritionally compromised hosts. Journal of Infectious Diseases 182 (Suppl 1):S108-114.

6.  Gulland FMD, K Beckmen, K Burek, L Lowenstine, L Werner, T Spraker, M Dailey, E Harris. 1997. Nematode (Otostrongylus circumlitus) infestation of northern elephant seals (Mirounga angustirostris) stranded along the central California coast. Marine Mammal Science 13(3):446-459.

7.  Measures, LN 2001. Lungworms of marine mammals. In: Samuel, W.M., M.J. Pybus, and A.A. Kocan (eds.) Parasitic Diseases of Wild Mammals, 2nd ed. Iowa state University, Press, Ames, Iowa. Pp. 279-300.

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Kathleen M. Colegrove

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