Juvenile, female Northern elephant seal, Mirounga angustirostrisThe seal was found stranded in California. On physical exam, it was found to be blind and had bilateral cataracts. It spent 8 months in a stranding center and was later sent to Adventure Aquarium in Camden, NJ. The seal did well, but a week after arrival it was found floating and unresponsive following administration of 4 tabs (large dog size) of Drontal. The seal was known to be Toxoplasma gondii positive.
At necropsy, the animal had moderately decreased subcutaneous blubber thickness.Â The haircoat was extremely sparse and completely absent over much of the animal.Â There were numerous multifocal to coalescing cutaneous ulcers and erosions along the ventrum extending from the muzzle to the anus and on the ventral aspects of the fore and hind flippers.Â Both eyes had opaque, cataractous lenses.Â The teeth were covered with moderate to abundant dental calculus.Â A vascular anomaly involving the portal vein and caudal vena cava was identified.
Within the leptomeninges and surrounding blood vessels throughout the cortex, cerebellum and brainstem, there are multifocal aggregates of lymphocytes, plasma cells and histiocytes (Fig.Â 1-1).Â The surrounding parenchyma is rarefied and gliotic with neuronal chromatolysis and necrosis.Â Within some inflammatory foci are thin-walled tissue cysts up to 40 x 60 um, that contain numerous 1-2 um elongate bradyzoites consistent with T.Â gondii (Fig.Â 1-2).Â A few necrotic foci with moderate lymphohistiocytic inflammation and associated tissue cysts are observed within sections of skeletal muscle.Â Individual tissue cysts without associated inflammation or necrosis are present in the ovary and in the wall of a medium sized myocardial artery.Â
Brain: meningoencephalitis, necrotizing and lymphohistiocytic, multifocal, moderate to severe with protozoal cysts consistent with T.Â gondii.Â
Immunohistochemistry: Toxoplasma gondii antibody applied to sections of brain revealed strong positive staining of bradyzoite cysts for Toxoplasma gondii antigen (Fig.Â 1-3).Â No definitive staining of cysts or tachyzoites was seen in the skin lesions.
Toxoplasma gondii is a coccidian parasite that is found throughout the world and infects an extensive range of intermediate hosts in which it causes both clinical and more commonly, subclinical disease.(7) Domestic and wild felids are the only known definitive hosts and also serve as intermediate hosts.Â
Infection occurs by ingestion of sporulated oocysts excreted in the feces of felids, by ingestion of tissues of intermediate hosts that contain encysted bradyzoites or tachyzoites, and less frequently by vertical transmission.Â Once ingested, sporozoites excyst and multiply in the intestinal epithelial cells as tachyzoites.Â Tachyzoites can either disseminate and infect cells throughout the body resulting in the necrosis and non-suppurative inflammation characteristic of toxoplasmosis, or encyst in tissues as bradyzoites.Â Following ingestion of tissue cysts by an intermediate host, bradyzoites will excyst, become tachyzoites, and the cycle continues.(2,6,7)
There is one report of toxoplasmosis in an elephant seal pup.Â (4) Microscopic lesions included multifocal non-suppurative meningoencephalitis and multiple tissue cysts with and without associated inflammation in the cerebrum.Â Cyst morphology was consistent with T.Â gondii, and protozoa stained positively with T.Â gondii, but not with N.Â caninum, polyclonal antibody.Â Focal lymphoplasmacytic inflammation was present in the brain, retina, optic nerve and renal tubules, and non-suppurative glossitis with necrosis and ulceration was also observed.(4)
Toxoplasmosis in marine mammals has recently become of particular concern since being identified as a leading cause of encephalitis and death in the threatened Southern sea otter (Enhydra lutris nereis).(8) Since 1951, toxoplasmosis has been reported in various species of seals, dolphins, a sea lion, a West Indian manatee and a beluga whale.(5) Serological assays of numerous species of marine mammals suggests common and widespread exposure.Â (5)
It is unclear how marine mammals become infected with T.Â gondii as they rarely consume recognized intermediate hosts, and T.Â gondii is not known to parasitize fish or invertebrates.Â It has been proposed that infection occurs through consumption of oocysts that enter the marine environment via surface run-off or municipal sewage contaminated by cat feces.(9,11) In support of this theory, T.Â gondii oocysts have been shown to sporulate and survive in seawater for several months.Â (9) Laboratory experiments have shown that bivalves can concentrate T.Â gondii oocysts (9) and recently, a wild California mussel was confirmed positive for T.Â gondii(10) suggesting that invertebrate filter feeders can serve as a source of infection for marine mammals.Â Additionally, a type X strain of T.Â gondii that has recently been isolated in over 72% of all sea otter infections(2) was identified in the California mussel as well as in several coastal dwelling felids and canids.(10)
Cerebrum; brainstem: Meningoencephalitis, necrotizing, histiocytic, multifocal, mild with lymphoplasmacytic perivascular cuffing and few protozoal cysts, Northern elephant seal (Mirounga angustirostris), pinniped.
Toxoplasma gondii is a ubiquitous organism that is indiscriminate in nature, infecting all warm-blooded animals, but members of the family Felidae are the only known definitive hosts.Â (6) Systemic disease occurs mostly in young or immunocompromised animals, and a lack of proper macrophage function in these neonatal animals contributes directly to this outcome.Â (1) Toxoplasma can infect many different cell types, and this leads to rapid dissemination throughout the host.Â It can infect many different leukocytes to include macrophages, lymphocytes, and granulocytes and be carried in the bloodstream or in lymph via a cell carrier or independently in plasma.Â (1) Toxoplasma then enters a host cell by active penetration of the host cell-membrane and can contort itself in multiple ways to achieve entry into the cell.Â Once in the cell, the tachyzoite changes shape to from a more ovoid structure and is surrounded by a parsitophorous vacuole that protects it from the hosts immune response.(7) Tachyzoites multiply with the parasitized cell, eventually killing it, with subsequent movement to adjacent cells within the resident organ resulting in the characteristic necrotizing lesion often seen with toxoplasmosis.Â Cell mediated immunity seems to be the more important that humoral immunity, and over time animals develop a quiescent infection characterized by cysts with a thin outer wall containing numerous bradyzoites, which are more slender and less susceptible to destruction by proteolytic enzymes than tachyzoites.(1)
Numerous organ systems are affected by toxoplasmosis, with pulmonary lesions and central nervous system lesions having the highest prevalence.(1) Within the lung, lesions are characterized by necrosis of alveolar walls, bronchiolar epithelium, and the vasculature with an accompanying interstitial pneumonia with mononuclear cell invasion into the alveolar walls.(1) Multifocal necrosis within the central nervous system and accompanying non-suppurative inflammation can occur with toxoplasmosis.Â Microglial nodules are occasionally seen with chronicity within the parenchyma of the central nervous system.(1)
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3.Â Dubey JP: Toxoplasmosis-a waterborne zoonosis.Â Vet Parasitol 126:57-72, 2004
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6.Â Gardiner CH, Fayer R, Dubey JP: Apicomplexa Toxoplasma and Hammondia.Â In: An atlas of protozoan parasites in animal tissues, 2nd ed., pp.Â 53-56.Â Armed Forces Institute of Pathology, Washington, DC 1998
7.Â Hill DE, Chirukandoth S, Dubey JP: Biology and epidemiology of Toxoplasma gondii in man and animals.Â Animal Health Research Reviews 6:41-61, 2005
8.Â Kreuder C, Miller MA, Jessup DA, Lowenstine LJ, Harris MD, Ames JA, Carpenter TE, Conrad PA, Mazet JAK: Patterns of mortality in Southern sea otters (Enhydra lutris nereis) from 1998-2001.Â J Wildl Dis 39:495-509, 2003
9.Â Lindsay DS, Collins MV, Mitchell SM, Cole RA, Flick GJ, Wetch CN, Lindquist A, Dubey JP: Sporulation and survival of Toxoplasma gondii oocysts in seawater.Â J Eukaryot Microbiol 50:687-8, 2003
10.Â Lindsay DS, Collins MV, Mitchell SM, Wetch CN, Rosypal AC, Flick GJ, Zajac AM, Lindquist A, Dubey JP: Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica).Â J Parasitol 90:1054-1057, 2004
11.Â Miller MA, Gardner IA, Kreuder C, Paradics DM, Worcester KR, Jessup DA, Dodd E, Harris MD, Ames JA, Packham AE, Conrad PA: Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis).Â Int J Parasitol 33:997-1006, 2002
12.Â Miller MA, Miller WA, Conrad PA, James ER, Melli AC, Leutenegger CM, Dabritz HA, Packham AE, Paradics DM, Harris M, Ames J, Jessup DA, Worcester K, Griggs ME: Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: New linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters.Â Int J Parasitol article in press, 2008