JPC SYSTEMIC PATHOLOGY
DIGESTIVE SYSTEM
October2021
D-P23

 

Signalment (JPC #1692806):  6-year-old ox

 

HISTORY:  Liver was condemned at slaughter

 

HISTOPATHOLOGIC DESCRIPTION:  Liver:  Effacing and replacing 75% of the hepatic parenchyma in this section and distorting the hepatic architecture are multifocal to coalescing, variably sized (up to 6 mm in diameter) trematode migration tracts that contain numerous elliptical, 170 x 100 um, operculated trematode eggs that have a 4 um thick, yellow-brown shell and contain eosinophilic flocculant material.  Eggs are admixed with abundant eosinophilic cellular and karyorrhectic debris (lytic necrosis) and moderate amounts of green to black, anisotropic, granular pigment (iron-porphyrin fluke pigment), basophilic mineral, small amounts of fibrin, hemorrhage, edema, and cholesterol clefts.  These migration tracts are bounded by numerous eosinophils, macrophages, lymphocytes, and plasma cells; these are further bounded by a dense fibrous capsule that compresses the adjacent parenchyma.  Adjacent hepatocytes have microvacuolated cytoplasm (vacuolar degeneration, glycogen type) and there is occasional individual hepatocyte death.  Remaining portal areas are infiltrated by lymphocytes, plasma cells, and eosinophils, contain moderate amounts of black fluke pigment, and there are increased biliary duct profiles (ductular reaction). 

 

MORPHOLOGIC DIAGNOSIS:  Liver:  Hepatitis, necrotizing, nodular, and eosinophilic, multifocal to coalescing, marked, with iron-porphyrin pigment, biliary hyperplasia, fibrosis, and numerous trematode eggs, breed unspecified, bovine.

 

ETIOLOGIC DIAGNOSIS:  Hepatic fascioloidiasis

 

CAUSE:  Fascioloides magna

 

GENERAL DISCUSSION:

• Large liver fluke (10cm long, 2-4.5mm thick, 3cm wide) that lacks an anterior projecting cone
• Important pathogen of sheep, goats, and cattle
• Adult flukes reside in parasitic tracts within the liver parenchyma (not in bile ducts)
• Spores of Clostridium novyi and Clostridium hemolyticum can become activated by the anaerobic necrotic conditions created in the liver parenchyma by migrating flukes in sheep and cattle

 

PATHOGENESIS:

• Definitive hosts: Cervids (elk, white-tailed deer, caribou)
  • Thin-walled fluke cyst lumen communicates with the bile duct and often contains breeding pair
  • Eggs are passed in the feces
  • Not pathogenic to host
• Dead-end hosts: Bovids; moose
  • Freely living or encysted; fluke cyst does not communicate with the bile duct
  • Fibrosis often prevents eggs from leaving the host
  • Parasite will not mature fully without a mate
  • Rarely causes illness in bovids, moose; however, a recent report indicates that magna is an important cause of morbidity and mortality in affected moose populations (Shury, Vet Pathol. 2019)
• Aberrant hosts: Ovine and caprine
  • Migrates freely around the liver in search of a mate
  • Severe hepatic damage, hemorrhage, and death to host

 

LIFE CYCLE:  Indirect

• The intermediate host is the lymnaeid snail:
• Requires a moist, warm habitat and temperatures above 50⁰F to breed
  • Summer infection of snail: Miracidia hatch from eggs in spring/summer and contaminate herbage 5-8 weeks later
  • Winter infection of snail: Snails are infected in the fall but fluke development ceases until temperatures rise in the spring
• Egg deposited in feces via biliary duct > hatch in 9 days (warm temperature, moisture dependent) as free-living ciliated larvae (miracidia) > ingested by lymnaeid snail (IH) > sporocyst > rediae (asexual) > cercariae (leaves IH) > encysts on green plants as metacercariae (infective) > ingested by DH or aberrant host > activation and excystment in the duodenum > penetrate intestine to peritoneal cavity (3-4 weeks) > invade liver

 

TYPICAL CLINICAL FINDINGS:

• Cervids: Asymptomatic, mild anemia, poor condition with large fluke burdens
• Bovids: Asymptomatic, weight loss, decreased milk production, pallor, submandibular edema, anorexia, depression in severe cases
• Sheep/Goats:
  • Acute syndrome: sudden death or fever, dullness, weakness, inappetence, and abdominal tenderness progressing quickly to death
  • Subacute syndrome: weight loss, pallor of mucous membranes, +/- submandibular edema, abdominal tenderness

 

TYPICAL GROSS FINDINGS:

• Cervids:
  • 2-5cm, yellow-white, thin-walled, fibrous cysts that contain two or more flukes
  • White, fibrous migration tracts and black pigment in chronic cases
  • Migration tracts possible in the lungs and other organs
• Bovids:
  • Necrotic tracts in liver
  • 2-5cm cysts with abundant black pigment surrounded by fibrosis
  • Scarring of migration tracts
  • Occasionally similar nodules/abscesses are present with flukes in aberrant locations, especially within the lung, near the peripheral portion of the pleura
• Sheep:
  • Extensive black, necrotic, hemorrhagic, tortuous migration tracts throughout hepatic parenchyma
  • +/- peritonitis with heavy and repeated infestations

 

TYPICAL LIGHT MICROSCOPIC FINDINGS:

• Cervids:
  • Similar lesions to bovids, but less accumulation of eggs and pigment
  • Thin-walled cysts communicate with bile ducts
• Bovids:
  • Multiple hepatic granulomas with trematode eggs (thick-walled, operculated, yellow-brown, anisotropic)
  • Deposits of jet black iron-porphyrin pigment, eosinophils, and abundant fibrous connective tissue
  • Pyogranulomatous migration tracts throughout liver
• Sheep:
  • Severe neutrophilic, eosinophilic, hemorrhagic, necrotizing reaction surrounding migrating flukes
  • Little fibrosis
  • May invade vasculature causing vasculitis and thrombosis

 

ADDITIONAL DIAGNOSTIC TESTS:

• Ova in feces
• Identification of parasites and/or eggs in the liver

 

DIFFERENTIAL DIAGNOSIS:

• Fasciola hepatica (common liver fluke)
  • Affects cattle and sheep in cooler climates
  • Flukes live in bile ducts > cholangiohepatitis with hyperplasia and epithelial erosions
  • Bile ducts are thickened by fibrosis and calcification (“pipe-stem liver”)
  • Most flukes reach bile ducts but some become encysted in the parenchyma
  • Can infect humans (usually via ingestion of marsh plants such as watercress)
• Fasciola gigantica (large African liver fluke)
  • Similar to hepatica but three times larger; in bile ducts
  • Affects cattle and sheep in Africa, SE Asia, southern US, Europe, and Hawaii (warmer climates)
  • Adults are 75mm x 12mm
• Dicrocoelium dendriticum (D-P27, old world or lancet fluke)
  • Common in Europe and Asia; found in dry lowlands or mountain pastures
  • Flukes in bile ducts of cattle, sheep, goats, horses, camels, cervids, pigs, dogs, rabbits, rodents and humans
  • Adults are small, 5-12mm long, 1mm wide, and lancet shaped
  • Hyperplasia and erosions of the bile duct epithelium, walls thickened and surrounded by fibrosis; liver parenchyma usually spared

 

COMPARATIVE PATHOLOGY:  Liver flukes in other species:

• Opisthorchis sinensis (Clonorchis sinensis):
  • Dogs, cats, pigs, NHP
  • Orient
  • Associated with cholangiocarcinoma in NHPs
• Opisthorchis felineus (Lanceolate fluke):
  • Bile ducts of cats, dogs, and foxes
  • Europe and Russia
• Pseudamphistomum truncatum:
  • Carnivores and humans
  • Europe and Asia
• Athesmia foxi: Adults in the bile ducts of new world monkeys
• Metorchis conjunctus:
  • Adults in bile ducts
  • Cholangiohepatitis in fish-eating mammals (dogs, cats, foxes, mink)
  • Common liver fluke in North America
  • Important in sled dogs in the Canadian Northwest Territories
• Metorchis albidis: Alaskan dogs
• Metorchis bilis: Red fox and occasionally cats from Germany
• Paramethorchis complexus: Cats in the U.S.
• Amphimerus pseudofelineus: Cats and coyotes in the U.S. and Panama
• Platynosomum fastosum: Adults in liver and bile ducts of cats in North America and the Amazonian regions of South America
• Opisthorchis tenuicollis: Adults in pancreatic and bile ducts of dogs, cats, foxes and pigs
• Eurytrema pancreaticum or E. coelomaticum: Adults in pancreas but with heavy infections can be found in bile ducts of cattle and sheep
• Eurytrema procyonis (Concinnum procyonis): Adults in pancreatic and bile ducts of fox and raccoons in the U.S.
• Dicrocoelium dendriticum: Flukes in bile ducts of cattle, sheep, goats, horses, camels, cervids, pigs, dogs, rabbits, rodents and humans; in camelids can induce pulmonary artery hypertensive lesions in addition to liver damage (Hilbe, Vet Pathol. 2015)

 

REFERENCES:

1. Agnew D. Camelidae. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals, Cambridge, MA Academic Press; 2018: 200.
2. Brown DL, Van Wettere AJ, Cullen JM. Hepatobiliary System and Exocrine Pancreas. In: Pathologic Basis of Veterinary Disease. 6^th St. Louis, MO: Elsevier; 2017:446-447.
3. Constable PD, Hinchcliff KW, Done SH, Grunberg W. Veterinary Medicine: A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs and Goats. 11th ed.  Louis, MO: Elsevier; 2017:641-645.
4. Higgins D, Rose K, Spratt D. Monotremes and Marsupials. In: Terio KA, McAloose D, St. Leger J, ed. Pathology of Wildlife and Zoo Animals, Cambridge, MA Academic Press; 2018: 473.
5. Hilbe M, Robert N, Popischil A, Gerspach C. Pulmonary arterial lesions in new world camelids in association with Dicrocoelium dendriticum and Fasciola hepatica Vet Pathol. 2015;52(6):1202-1209
6. Lee JK, Rosser TG, Cooley J. Pulmonary embolization of immature Fascioloides magna causing fatal hemothorax confirmed by molecular technique in a heifer in the United States. J Vet Diagn Invest. 2016;28(5): 584-588.
7. Miller MA, Zachary JF. Mechanisms and Morphology of Cellular Injury, Adaptation, and Death. In: Pathologic Basis of Veterinary Disease. 6^th St. Louis, MO: Elsevier; 2017: 38-39.
8. Pybus MJ, Butterworth EW, Woods JG. An expanding population of the giant liver fluke (Fascioloides magna) in elk (Cervus Canadensis) and other ungulates in Canada. J Wildlife Dis. 2015;51(2):431-445.
9. Reissig EC, Massone AR, Iovanitti B, Gimeno EJ, Uzal FA. A survey of parasite lesions in wild red deer (Cervus elaphus) from Argentina. J Wildl Dis. 2018; 54(4): 782-789.
10. Shury TD, Pybus MJ, Nation N, Cool NL, Rettie WJ. Fascioloides magna in Moose (Alces alces) from elk island national park, Alberta.  Vet Pathol. 2019; 56(3): 476-485.
11. Uzal FA, Plattner BL, Hostetter JM. Alimentary system. In: Maxie MG, ed. Jubb, Kennedy and Palmer’s Pathology of Domestic Animals. Vol 2. 6th ed. St. Louis, MO; Elsevier; 2016:320-324.

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