Acute coenurosis in lambs

Abstract

Six 100-day-old mixed-breed lambs were examined in a farm with a semi-intensive system due to neurologic signs. Cachexia, bilateral blindness, stupor, severe drowsiness and lethargy with left and right movements of the head and neck were recorded after awakening and stimulation. Lambs died 10 days after the onset of the clinical signs. The lambs were necropsied, and after routine parasitology, bacteriology and histopathology, the occurrence of acute coenurosis was confirmed due to finding multiple cystic structures in the brain tissue. All lambs of the herd were treated with albendazole (orally, 25 mg/kg, two doses with an interval of 14 days). All shepherd dogs were treated with popantel (orally, one tablet/10 kg, two doses with an interval of 14 days). The affected lambs died despite this treatment. No new case of the disease was observed after the initiation of control measures. The present study shows the importance of preventive measure against coenurosis in a semi-intensive sheep farming system that includes implementing consistent parasite control programme in dogs being in contact with sheep.

INTRODUCTION

Coenurosis (Gid) (Sturdy) is a zoonotic neurological disease (Abera et al., 2016; Deplazes et al., 2019). This disease is one of the concerns of the small ruminants breeding industry (Abbas et al., 2022; Abera et al., 2016). The cause of this disease is Coenurus cerebralis, the larval stage of the Multiceps multiceps (Taenia multiceps) tapeworm (Miran et al., 2015; Scala et al., 2007). M. multiceps lives in small intestine of the definitive host's (dog and wild Canidae). C. cerebralis lives in brain, visceral organs, muscle and subcutaneous tissue of the intermediate hosts (sheep, goat, cow, camel, yak, wild sheep, human, deer, pig and horse) (Azizi et al., 2019). Coenurosis has two forms, that is acute and chronic, whose chronic form is much more common and is caused by cerebral, visceral, muscular and subcutaneous C. cerebralis cysts containing cluster protoscoleces (Azizi et al., 2019; Christodoulopoulos et al., 2016; Varcasia et al., 2022). The acute form of coenurosis is rare and occurs due to simultaneous cerebral migration of large numbers of C. cerebralis oncospheres (larvae less than 5 mm in diameter) (Abera et al., 2016; Varcasia et al., 2022). The present study describes an occurrence of acute coenurosis in the weaned lambs in a semi-intensive system.

CASE DESCRIPTION Clinical presentation

This study was conducted in October 2022 in a rural semi-intensive sheep farm (Tuye-Darvar village, Damghan city, Iran) with thirty 100-day-old mixed-breed male lambs. This farm was examined after complaining about stupor of six lambs. The affected lambs were separated from their mother 20 days ago, and taken to the new farm for fattening in a semi-intensive system. Clinical examinations of the affected lambs showed cachexia, bilateral blindness, stupor (Figure 1a), severe drowsiness and lethargy with left and right movements of the head and neck after awakening and stimulation. Other clinical examination findings were normal. The duration of the disease was 10 days, and it seemed that the animals died due to hunger and weakness. Three died lambs were examined by necropsy, histopathology and bacteriology. There were five shepherd dogs in the farm, and no antiparasitic treatment had been done on the dogs.

Necropsy

Multiple linear reddish-yellow foci of necrotic purulent inflammation on the surface of the brain (indicative of parasitic larvae migration) (Figure 1b), hyperaemia of the vessels on the surface of the brain, softness of the cerebral cortex and laxity of the brain white matter, were recorded. In one of the affected lambs, there was a 2 mm cyst on the leptomeninges (Figure 1b).

Histopathologic examination

The brain samples were also taken in 10% neutral buffered formalin for histopathological examination. The samples were routinely processed for histopathological evaluation as follows: dehydrated, embedded in paraffin wax, sectioned at 5 μm thickness using a rotary microtome (RM2 145; Leica) and stained with haematoxylin and eosin (H&E). The histopathologic examination of the brain tissue sections (H&E) showed that multiple cystic structures with finger-like projections were observed in the brain tissue. The cysts walls were composed of a translucent proteinous membrane, and most of the cysts contained eosinophilic and proteinous materials. These cysts were surrounded by inflammatory cells (especially lymphocytes and plasma cells) (Figure 2a–c). In microscopical examination, granulomatous inflammation was also observed in the brain. The granulomas were round to oval. They were composed of a central core of cell debris, surrounded by a dense zone of macrophages and giant cells that were admixed increasingly in the outer layers of granuloma with lymphocytes, plasma cells and fibroblasts (Figure 2d,e). There were the prominent perivascular cuffs of small mononuclear cells and macrophages in the brain tissue (Figure 2f). Finally, cystic and granulomatous encephalitis were diagnosed.

Parasitologic examination

The 2 mm cyst was taken in 70% ethanol for parasitologic examination. For PCR, DNA was extracted from the cyst sample using the DNA extraction kit (Sinaclon). The DNA was used for PCR amplification of cytochrome c oxidase subunit I (CO1). As shown in Figure 1c, the amplified part of the CO1 gene with specific primers (F: 5′-TTTTTTGGGCATCCTGAGGTTTAT-3′, R: 5′-TAAAGAAAGAACATAATGAAAATG-3′) showed the expected product size of 400 bp at the agar gel electrophoresis indicating the presence of M. multiceps DNA in the brain samples (Rostami et al., 2013).

Bacteriologic examination

The brain samples were sent to the laboratory for aerobic and anaerobic cultivation, next to an ice bag. Aerobic and anaerobic bacterial cultures of the brain samples were negative.

Treatment

All lambs of the farm were treated with albendazole (orally, 25 mg/kg, two doses with an interval of 14 days). All shepherd dogs were treated with popantel (orally, one tablet/10 kg, two doses with an interval of 14 days). The affected lambs (three lambs) died despite this treatment. No new cases of the disease were observed after the initiation of control measures.

DISCUSSION

Based on the results of diagnostic, therapeutic and control measures, the occurrence of acute coenurosis in the studied lambs was confirmed. Shepherd dogs were considered the suspected source of infection. The disease was controlled by administration of albendazole in the remaining lambs and popantel (fenbendazole + praziquantel) in shepherd dogs.

In this study, diagnosis of acute coenurosis was based on histopathology. In histopathology, multiple cystic structures with finger-like projections, granulomatous inflammation and the prominent perivascular cuffs of small mononuclear cells and macrophages in the brain tissue were very helpful. At necropsy, in all the examined brain samples, multiple linear reddish-yellow foci of necrotic purulent inflammation (indicative of parasitic larvae migration) in some parts of the cerebral surface, mild leptomeninges vessels congestion, softness of the cerebral cortex and laxity of the white matter of the brain were observed but one macroscopic leptomeningeal cyst with a diameter of 2 mm was observed only in one of the patients. It was interesting that in the histopathology sections of the brain, multiple cysts like structures (Figure 1d) were easily visible with the naked eye in each slide section. In all the reports reviewed by researchers about the acute form of coenurosis, the diagnosis was made by necropsy and histopathology methods (Farjani Kish et al., 2015; Giadinis et al., 2012; Hobbenaghi et al., 2014; Pintus et al., 2018).

During the study of Giadinis et al. (2012), seven outdoor herds and four indoor herds in central and northern Greece were studied for 1 year. In this study, 42 animals with acute coenurosis were identified, 13 of which were subjected to gross pathology, histopathology and bacterial brain culture. In gross pathology, the predominant finding was 0.5–1 cm cysts, but in the present study, only one 2 mm cyst was observed in the brain of one patient. The histopathological finding of this study was pyogranulomatous meningoencephalitis, and in the present study, in addition to granulomatous encephalitis, multiple microcysts were also observed in brain tissue sections. In Giadinis's study and also the present study, the bacterial cultures of the infected brain were negative.

In the study of Hobbenaghi et al. (2014), the occurrence of acute neurological signs was investigated in 30 sheep. The diagnosis of acute coenurosis was occurred at necropsy. There were cystic structures with a diameter of 5–10 mm in the cerebrum leptomeninges of the patients.

In the study of Farjani Kish et al. (2015), the occurrence of acute neurological signs was investigated in 30 sheep. The diagnosis of acute coenurosis was occurred at necropsy. There were focal to multifocal necrotic areas and whitish spots measuring 1–3 cm in diameter in the cortex of cerebrum and cerebellum.

Pintus et al. (2018) studied the occurrence of acute coenurosis in a semi-intensive flock with 600 adult ewes and 30 lambs (aged between 1 and 30 days) in Sardinia (Italy). In Pintus's study, 28 animals aged 25 days to 6 months were affected, whereas in the present study, 6 lambs aged 100 days (after weaning and entering the new pasture) were affected. In Pintus's study, clinical findings in patients included teeth grinding, ataxia, lateral recumbency and head tilt to the side, whereas in the present study, clinical findings in patients included cachexia, bilateral blindness, stupor, severe drowsiness and lethargy with left and right movements of the head and neck after awakening and stimulation. In Pintus's study, gross anatomo-pathological inspection findings in patients included multiple linear reddish-yellow foci of necrotic purulent inflammation indicative of parasitic larvae migration and parasitic cysts (12–15 mm wide) in the leptomeninges of the adult sheep brains, whereas in the present study, in addition to the presence of multiple linear reddish-yellow foci of necrotic purulent inflammation in the brain of all patients, a small cyst (2 mm wide) was observed in the leptomeninges of one lamb. The histopathological findings of Pintus's study were pyogranulomatous meningoencephalitis, perivascular cuffing and empty cysts in brain tissue sections, whereas in the present study, in addition to these findings, multiple microcysts were also observed in brain tissue sections. In Pintus's study, like the present study, shepherd dogs in the farm, which had no history of antiparasitic treatment, were considered suspected source of infection.

In Varcasia et al. (2022) study, it has been mentioned that lambs with acute coenurosis die within 3–5 days, but in this study, the survival time of the affected lambs varied between 10 days. In this study, it seemed that the main cause of death was secondary consequences, such as weakness, blindness and inability to receive food. Although the survival time was shorter in Varcasia's study, this finding was normal in our study considering the difference in the location of parasite lesions in the brain.

Albendazole drug (25 mg/kg) was used to treat the affected lambs based on the recommendations (Oryan et al., 2014; Varcasia et al., 2022). The administration of this drug was not effective in the treatment of the patients, although it seemed that starvation and weakness due to blindness were the cause of death of the affected lambs.

Disease control was done in two stages. In the first stage, remaining lambs in the group were treated with albendazole (orally, 25 mg/kg, two doses with an interval of 14 days). In the second stage, shepherd dogs were treated with popantel (orally, one tablet/10 kg, two doses with an interval of 14 days). After these two measures, no new cases of the disease were observed.

CONCLUSIONS

According to the present study and discussion, it was shown that acute coenurosis in lambs was a lethal, acute and insidious disease. Necropsy of the dead lambs may allow for early diagnosis and intervention for the remainder of the herd. This disease can be controlled by early treatment of the residual lambs. Prevention of acute coenurosis includes implementing consistent parasite control programmes in dogs that are in contact with sheep.

AUTHOR CONTRIBUTIONS

Conception and design; collecting the data; sampling; writing and revising the article: Mostafa Abdollahi. Conception; sampling; writing the article: Samad Lotfollahzadeh. Assistance in laboratory work; writing the article: Sara Shokrpoor. Assistance in laboratory work: Mojtaba Daneshi. Assistance in laboratory work: Moein Abolhasani Darounkola.

ACKNOWLEDGEMENTS

Mr Ali Damghani, the owner of Tuye farm, is appreciated for her cooperation in this research.

CONFLICT OF INTEREST STATEMENT

The authors declare that there are no conflicts of interest.

FUNDING INFORMATION

There is no source of fund to declare.

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available within the manuscript and also are available from the corresponding author upon reasonable request.

ETHICS STATEMENT

The authors confirm that the ethical policies of the journal, as noted on the journal's author guidelines page, have been adhered to and the appropriate ethical review committee approval has been received.

PEER REVIEW

The peer review history for this article is available at https://publons.com/publon/10.1002/vms3.1278.