Acute cysticercosis caused by Cysticercus tenuicollis in lambs

Abstract Twelve 30‐ to 75‐day‐old mixed breed lambs were examined in an intensive system because of sudden recumbency and death. Clinical examination revealed sudden recumbency, visceral pain, and auscultation of respiratory crackles. Lambs died shortly (between 30 minutes and 3 hours) after the onset of clinical signs. The lambs were necropsied, and after routine parasitology, bacteriology and histopathology procedures, the occurrence of acute cysticercosis caused by Cysticercus tenuicollis was confirmed. The use of the suspect infested feed (newly purchased starter concentrate) was discontinued and other lambs of the flock were treated with praziquantel (15 mg/kg, single dose, orally). After these actions, no new cases were observed. The present study showed the importance of preventive measures against cysticercosis in intensive sheep farming systems which include proper storage of feed, preventing feed and environmental access by potential definitive hosts, and implementing consistent parasite control programs in dogs that are in contact with sheep.


| INTRODUCTION
Cysticercosis is a disease caused by a cysticercoid, with Cysticercus tenuicollis being 1 of the most common etiologies in small ruminants.
Cysticercus tenuicollis is the larval stage (metacestod) of the Taenia hydatigena tapeworm. 1,2 Mature, egg-containing proglottids are shed in the feces of the definitive host. 1 The proglottids disintegrate in the environment and the eggs are released. The intermediate hosts (sheep, goat, cow, deer, pig, and horse) ingest eggs. The oncosphere larva is freed from the egg in the intermediate host and penetrates into its organs. 2 Cysticercus tenuicollis metacestodes are typically formed in the omentum or liver. 3 The geographical distribution of this parasite is worldwide. 4 Cysticercosis caused by C. tenuicollis has, acute and chronic forms. Its chronic form is much more common, usually asymptomatic, and it is identified in the slaughterhouse as large larval cysts (benign cysts) on the omentum, mesentery, peritoneum and, less frequently, in the pleura and pericardium. 3,5 The acute form of cysticercosis, because of C. tenuicollis, is a rare condition and usually results in death because of parasitic hepatitis, caused by the simultaneous migration of a large number of growing cysticercoids. 5 The present study describes an occurrence of acute cysticercosis in the suckled lambs in an intensive management system.

| Necropsy
Worm-shaped hemorrhages under the liver capsule ( Figure 1A), fibrin deposition on the liver ( Figure 1B), pinpoint hemorrhages in the liver ( Figure 1C), and lung congestion were recorded. Colorless pomegranate seed-like larvae were seen in the liver parenchyma ( Figure 1D), on the lung surface ( Figure 2A) and in the abdominal cavity (under the liver) ( Figure 2B).

| Parasitological examination
The isolated larvae were sent to the laboratory in 10% neutral buffered formalin for further investigation. The usual carmine staining method was used to identify parasite larvae. In the parasitological examination, immature C. tenuicollis ( Figure 3A) was identified. These larvae were cystic structures with a length of 4 mm and a width of 2 mm and they had a mouth in the front part.

| Histopathologic examination
The liver samples were placed in 10% neutral buffered formalin for histopathological examination. The samples were routinely pro-

Accumulation of inflammatory cells (especially mononuclear cells)
was observed around the parasite larvae ( Figure 4B). Infiltration of fibrocytes, fibroblasts, and collagen was also seen around these inflammatory cells ( Figure 4C). There were large numbers of macrophages containing hemosiderin in the vicinity of the larvae in the liver tissue ( Figure 4D).

| Bacteriologic examination
The liver samples were placed next to an ice bag, and sent to the laboratory for aerobic and anaerobic culture. Aerobic and anaerobic bacterial cultures of livers were negative.  area. Due to the lack of a history of acute cysticercosis in the study herd, the starter concentrate was considered the main suspected source of infection, and its use was discontinued.

| Treatment
Treatment of the remainder of the herd included the administration of praziquantel (15 mg/kg, single dose, orally). 6 After treatment was initiated, no additional cases were observed in the herd. It is reported that in a semi-closed herd with 120 Sarda sheep, 4 female lambs from a group of 21 lambs died because of acute C. tenuicollis hepatitis. 6 The lambs in this study were 60 days old at the time of diagnosis, and were placed in a pen at weaning (30 days of age)

| DISCUSSION
where several dogs had been kept for 15 days. The lambs were treated with praziquantel (15 mg/kg) after diagnosis. In treated lambs, 6 lambs were asymptomatic and 11 lambs had signs of lethargy and anorexia. In the treated lambs, only 1 lamb died and the rest recovered. 6 In the present study, unlike in another study, all lambs had peracute death and there were no preceding signs of lethargy or anorexia. 6 F I G U R E 4 (A) Another cross section of parasite larvae (arrowhead). (B) Infiltration of inflammatory cells especially mononuclear cells (arrowhead) and the connective tissue around the parasite (black line). (C) High magnification of the connective tissue around the parasite (arrow), hepatocytes (arrowhead). (D) Note the hemosiderin pigments in the macrophages around the hemorrhage site (arrow head). Routine H&E staining.
In a report of acute cysticercosis in Italy six 2-to 4-year-old goats and three 50-day-old goat kids died, and the pasture was considered as a possible source of infection. 8 In the present study, unlike other studies, all lambs were in the intensive system and did not have access to pasture. 7 Two occurrences of acute cysticercosis were reported because of C. tenuicollis in Israel. 8 In the first occurrence in a group of 90 lambs, 2 to 3-months-old, 36 lambs died over a 30-day period because of cysticercoid hepatitis caused by C. tenuicollis. The lambs did not have pasture access. There were no dogs on the farm and there was no dog access to the farm. Investigations showed that the feed purchased from a local dealer was the suspected source of infection, because other local sheep herds that had used the feed purchased from the dealer also developed the disease. Two lambs and 1 kid died by cysticercoid hepatitis and pneumonitis. The source of contamination was fresh forage of the land adjacent to the farm. 9 In the present study, like another study, the feed purchased from a dealer was considered the main suspected source of infection. 8 A study reporting acute cysticercosis in Greece 2 lambs, 2.5months-old died. 9 Another five lambs were necropsied at the veterinary clinic and the disease was diagnosed. Another 43 lambs were sent to the slaughterhouse, 20 of which showed signs of cysticercoid hepatitis on examination of the carcass. 10 In the present study, unlike another study, remainder of the herd included the administration of praziquantel and no additional cases were observed in the herd. 9 A study reported on 12 lambs with acute cysticercosis caused by C. tenuicollis which were diagnosed via ultrasound examination. 11 The livers of the lambs had round, thick, irregular, and hyperechoic edges.
Hepatic parenchyma had heterogeneous anechoic lesions (length 1-2 cm and width 0.2-1.2 cm). Intra-parenchymal cystic structures were also identifiable. Hepatic cysts were up to 0.4 cm in diameter and surrounded by damaged tissue. 11 In ultrasound examination, damaged tissues around the cysts were identified as heterogeneous parenchyma. In the present study, unlike another study, diagnosis was made using necropsy. 11 Eight lambs and 3 goat kids died in an outbreak in Iran. 12 At necropsy, cystic hepatitis caused by C. tenuicollis was detected. 12 In the present study, as in another study, a diagnosis was made using necropsy. 12

ACKNOWLEDGMENT
No funding was received for this study. Mr. Mahmood Mahmoudi is appreciated for assistance in sampling.