Prevalence and hepatic histopathological findings of fascioliasis in sheep slaughtered in Jeddah, Saudi Arabia

Abstract

Hepatic fascioliasis is an important parasitic disease responsible for morbidity and mortality in many domestic ruminants, especially sheep, goats, and cattle, due to Fasciola (F.) hepatica and F. gigantica. This study aimed to determine the prevalence of fascioliasis in sheep slaughtered in Jeddah, Saudi Arabia, and to describe the morphological and histopathological changes in the liver. A total of 109,253 sheep slaughtered between July 2017 and July 2018 were screened to assess the prevalence of fascioliasis. The livers were grossly investigated for Fasciola infection and morphological changes. Tissue samples were collected for proper histopathological examinations. Livers of local and imported sheep represented infection rates of 0.67% and 2.12%, respectively, and the highest infection rate was in the spring season. Macroscopically, the affected liver showed hepatomegaly, thickened capsule and discoloration with necrosis, fibrosis, dilation of the bile duct, engorgement of the gallbladder and enlargement of the portal lymph nodes. Microscopic examination showed fibrotic thickening, calcification and hyperplasia of the bile ducts filled with debris, as well as massive hemorrhagic foci. Histopathological examinations of the infected liver showed a central vein region with disturbed parenchyma cells, focal lymphocytic infiltration, elongated endothelial cells, blood sinusoids that showed enlarged Kupffer cells, patches of lysed or necrotic hepatocytes, eosinophil infiltration, lymphocytes and proliferating fibroblast, thickening of hepatic artery and arteriolar walls. We concluded that fascioliasis among sheep slaughtered in Jeddah is not uncommon. The identified histopathological changes in the liver of infected sheep reflect tissue damage, which can lead to significant economic losses for the animals.

Figure 1

Dimension of isolated liver flukes.

Figure 2

Correlation between seasons and rate of infection.

Figure 3

Normal liver morphology, (A: diaphragmatic surface view; B: visceral surface view). (C) The diaphragmatic surface of the infected liver showing lobular enlargements, thickened capsule (black arrows) and patches of fibrosis (dotted arrows). The migratory paths of worms can also be seen (dotted circles); (D) the visceral surface of the infected liver showing marked necrotic regions or abscess formation (dotted arrows). Note the engorgement of the gallbladder (white star), dilated bile ducts (asterisk) and enlarged portal lymph nodes (black stars); (E) mature and immature Fasciola flukes on the surface (black arrows), dilated bile ducts (black star) and enlarged portal lymph nodes (dotted arrows); (F) cut a section from infected liver showing fibrotic thickening and hyperplasia of the portal bile ducts (black arrows). Hemorrhagic foci (yellow star) were also presented; (G) cut a section from infected liver showing calcification and thickening of the bile ducts filled with debris (black arrows) and Fasciola fluke (dotted arrow) protruding from another bile duct can be seen.

Figure 4

Light microscopic photographs of non-infected sheep liver stained with H&E. (A) Central vein (CV) surrounded by hepatocytes (H), separated by sinusoids (S), lined with endothelial (dotted arrows) and Kupffer cells (arrows); (B) portal region with portal vein (PV), bile duct (black arrow) and hepatic artery (dotted arrow) with scanty connective tissues (black star). Note the normal feature of hepatocytes (H); (C) intact normal parenchyma (Pa) and normal thin Glisson's fibrous capsule (C) covered by intact mesothelial cells (M).

Figure 5

Light microscopic photographs of infected sheep liver stained with H&E. (A) Central vein (CV) region with disturbed parenchyma cells (Pa), focal lymphocytic infiltration (yellow stars), elongated endothelial cells (dotted arrows), enlarged Kupffer cells (arrow) and patches of lysed (necrotic) hepatocytes (dotted circle); (B) portal vein (PV) of the portal region with eosinophil and lymphocyte infiltration (arrows), the proliferation of bile ducts (dotted arrows) and lymphatic vessels (black stars). The adjacent liver parenchyma with patches of degenerating and lysed (necrotic) hepatocytes (dotted circles); (C) eosinophil infiltration, lymphocytes, and proliferating fibroblast (arrow), thickening of the hepatic artery (arrow heads) and arteriolar walls (yellow arrow heads), fibrosis (black stars), hyperplasia of bile ducts epithelium (dotted arrows) with damaged columnar epithelial and detached lining into the lumen (red star). The adjacent liver parenchyma (Pa) showed hepatocellular foci and lysis (dotted circles); (D) Glisson's thickened capsule (C), parenchyma fibrosis (yellow star) with sub capsular infiltrated inflammatory cells (arrows).

Figure 6

Light microscopic photographs of infected sheep liver stained with H&E. (A) thickened fibrous capsule (arrowhead) and capsule region of dark brownish hemosiderin pigment (arrows) with the marked proliferation of fibrous connective tissue (yellow stars). Inflammatory cells (dotted arrows) at the periphery of necrosed degenerated parenchymal hepatocytes (Pa); (B) part of dilated central vein (CV) with damage and loss of normal endothelial lining (dotted arrows). Note degenerated hepatocytes with dark stain nuclei (head arrows). Blood sinusoids showed enlarged Kupffer cells (dotted circle). Note massive hemorrhage at the site of necrotic hepatocytes (black arrow); (C) an adult fluke (arrow) in the lumen of the dilated bile duct (BD). Note the intact outer tegument (Ts) with embedded spines (Sp); (D) hyperplasia of the bile ducts (dotted arrows), extensive fibrosis of connective tissue (yellow stars) with heavy infiltration by various inflammatory cells (arrows). Note the presence of Fasciola worm (arrowhead) in the lumen of the dilated bile duct (BD). (E) Stained with Masson trichrome stain showing extensive fibrosis at portal region (yellow stars). Note the dilated lymphatic vessels (black stars), proliferated bile ducts (black arrows) and thickened walls of blood vessels (white arrows).