Signalment:  

One year old female Border collie (Canis familiars).This dog experienced chronic diarrhea that was often hemorrhagic, coupled with wasting. She was treated with various agents for giardiasis. She responded to treatment, then the diarrhea/wasting recurred. The dog was not brought in for further treatment. She was presented to the veterinarian several weeks later, and was extremely emaciated and anorexic, with severe, watery diarrhea. Euthanasia was elected rather than further treatment. Another dog (11 months old) in the household and had similar symptoms.

Gross Description:  

This young female Border collie was extremely thin, with no subcutaneous or internal body fat present. Terminal weight was 19.2 lbs. There was fecal pasting around the anus. The portal vein was markedly distended caudal to the liver and readily visible as it coursed caudad. The liver had a greenish tinge to the serosal surface and an accentuated lobular pattern, and was very firm on palpation. The heart was enlarged and rounded, with a developing double apex, and both ventricular walls were thin. The small intestine was distended with gas, and contents had a foul odor. There were aggregates of yellowish-brown mucoid material attached to mucosal surfaces in a random distribution.

Histopathologic Description:

Liver sections had severe and striking periportal fibrosis coupled with a mixed inflammatory infiltrate. Numerous trematode eggs were seen in portal regions; these had commonly induced a fibrotic response. Mixed inflammatory infiltrates composed of lymphocytes, plasma cells, and occasional eosinophils were seen, primarily in portal triads. There were also copious aggregates of brownish-black pigment granules deposited throughout the liver, most common in the portal triads. The small intestine (multiple sections) had copious numbers of trematode eggs embedded in the mucosa, submucosa, and extending into the muscularis in some areas (i.e., transmural distribution); these were surrounded by varying amounts of reactive fibroplasia and mixed inflammatory infiltrate forming microgranulomas. 

Morphologic Diagnosis:  

Liver: hepatitis, chronic, portal, nonsuppurative due to Heterobilharzia americana.

Small intestine: Enteritis, chronic, nonsuppurative, transmural, due to Heterobilharzia americana.

Lab Results:  

Parasitology - fecal samples from both dogs were positive for Heterobilharzia americana trematode eggs on fecal sedimentation test (Dr. Jack Malone, Louisiana State University, performed assay).

Condition:  

Heterobilharzia americana

Contributor Comment:  

This was a case of disseminated trematode infection due to Heterobilharzia americana, a schistosome trematode found in the southern US. Primary hosts include rabbits, raccoons and bobcats, all of which occur in the San Juan River Valley of northwestern New Mexico (i.e., "four corners" region of US). The fluke has essentially the same life cycle as Fasciola hepatica (also present in this area), and uses the same lymnaeid snail as part of its indirect life cycle.

In addition to the lesions in the tissues submitted, there were disseminated granulomas surrounding eggs in the pancreas, lung, lymph node, and kidney; the small intestine and liver were most severely affected.  The trematode is in the family Shistosomatidae; these parasites are of relatively low importance in North America. In addition to this trematode in dogs, there is a dermatitis of humans (i.e., "swimmer's itch") that is caused by a cercariae of wild waterfowl (Trichobilharzia, Austrobilharzia, and Bilharziella).(1)

The miracidium hatches very soon after the egg comes in contact with water, and then enters a freshwater snail (Lymnaea cubensis), in which cercariae develop in daughter sporocysts. Activity by these snails is dependent upon ambient temperatures between ranges of 10°C-29°C(4). If the ambient temperatures are within this range, development in the snail is completed within 30 days. Upon emergence from the snail, the cercariae penetrate the skin of the host (i.e., dog, rabbit, raccoon, bobcat, or nutria), and migrate by way of the lungs to the liver. After a period of development in the liver, mature males and females make their way to the mesenteric vein and mate. These adults do not reproduce in mammalian hosts, and but may live there for 4-10 years, producing thousands of eggs during that time.(6) Eggs laid in the terminal branches of the mesenteric veins passively work through the bowel wall via a mechanism of proteolytic enzymes that are emitted through an ultramicroscopic pore in the eggshell. They then progress to the gut lumen and escape in the feces. If feces are deposited in water, the process starts over again. The eggs evoke a granulomatous reaction that eventually prevents their egress, and favors their carriage to other organs with consequent production of widely disseminated granulomas.

It is of interest that fluke infestations, which are most often associated as problems in animals in a wet climate, can occur in a "high desert" climate and geographical environment such as the American Southwest. In the area involved, there is both flood irrigation and excessive water runoff situations during a summer wet or "monsoon" season. During these times, the necessary elements for this infection (as well as fascioliasis in cattle) are present, especially along the river bottoms or "bosque" zones. Of further interest is the involvement of the lymnaeid snail that is "double dipping" in trematode infections in several species with two different trematode parasites. 

JPC Diagnosis:  

1. Liver: Hepatitis, portal, granulomatous, diffuse, moderate, with numerous trematode eggs and nodular hemosiderosis. 
2. Small intestine: Enteritis, granulomatous, multifocal, moderate, with numerous mucosal and submucosal trematode eggs and intravascular adult schistosomes.

Conference Comment:  

As mentioned by the contributor, cercariae penetrate the skin and leave seldom seen petechiae with a marked leukocytic inflammatory response to the parasite. The cercariae develop into schistosomula and migrate through dermal vessels to the lungs, where a heavy parasite load can result in pneumonia. After migration to the liver, hepatic cirrhosis can result following healing of the granulomatous response to the eggs, leading to liver failure and gastrointestinal malabsorption. Common laboratory abnormalities reflect hepatic failure, widespread granulomatous disease, and parasitism, and include hypoalbuminemia, hyperglobulinemia, hypercalcemia, azotemia, anemia, and eosinophilia. Anemia reflects both enteric blood loss and chronic inflammatory disease. A reported sequel to schistosomiasis is membranoproliferative glomerulonephritis, due to the accumulation of antigen-antibody complexes within the glomerular capillary wall, which stimulates an inflammatory cascade leading to varying degrees of glomerular cell proliferation and basement membrane thickening. Clinical pathology abnormalities common in cases of glomerulonephritis include renal proteinuria, hypoalbuminemia, azotemia, and anemia(2,3). 

Diarrhea is a typical clinical finding attributed to rupture of enteric mucosal vessels and a type I hypersensitivity reaction that results in enteric ganglionitis. Small granulomas, called pseudotubercles, form in deeper tissues in chronic disease when endophebitis precludes escape of the eggs into the intestinal lumen, as discussed by the contributor. Pseudotubercles are initially primarily eosinophilic and later progress to traditional granulomas. With chronicity, degenerate eggs often mineralize or become coated with Splendore-Hoeppli material. Adult schistosomes elicit eosinophilic endophlebitis, intimal proliferation, and thrombosis in mesenteric and portal veins, as demonstrated in this case. Adults feed on erythrocytes and regurgitate hematin pigment, which was also evident in this case(5). Due to slide variation, not all sections of small intestine featured adult schistosomes in mesenteric vessels. 

References:

1. Bowman DD, Helminths: Georgi's parasitology for veterinarians (6th edition); pp.128-129. W. B. Saunders Co., Philadelphia (1995).
2. Fabrick C, Bugbee A, Fosgate G. Clinical features and outcome of Heterobilharzia americana infection in dogs. J Vet Intern Med. 2010 Jan-Feb;24(1): 140-4.
3. Flowers JR, et al. Heterobilharzia americana infection in a dog. J Am Vet Med Assoc. 2002 Jan 15;220(2): 193-6, 183.
4. Goff WL, Ronald WC: Certain aspects of the biology and life cycle of Heterobilhazia americana in east central Texas. ln: Am J Vet Res, vol. 42, no. 10, pp. 1775-1781 (1981).
5. Maxie MG, Robinson WF. Cardiovascular System. In: Maxie MG, ed. Jubb, Kennedy, and Palmers Pathology of Domestic Animals. Vol 3, 5th ed. Philadelphia, PA:Elsevier Saunders; 2007:95-7.
6. Slaughter JC, Billups LH, Acor GK: Canine heterobilharziasis. In: Compendium Small Animals, vol. 10, no. 5, pp. 606-61 1 (May 1988).

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