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Ultrasonography: An affordable diagnostic tool for precisely locating Coenurosis


cyst in sheep And goats

Article  in  Small Ruminant Research · October 2018


DOI: 10.1016/j.smallrumres.2018.10.002

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Accepted Manuscript

Title: Ultrasonography: an affordable diagnostic tool for


precisely locating Coenurosis cyst in sheep and goats

Authors: Hakim Athar, Mujeeb ur Rehman Fazili, Abdul


Qayoom Mir, Mudasir Bashir Gugjoo, Raja Aijaz Ahmad,
Hilal Musadiq Khan

PII: S0921-4488(18)30225-6
DOI: https://doi.org/10.1016/j.smallrumres.2018.10.002
Reference: RUMIN 5767

To appear in: Small Ruminant Research

Received date: 2-4-2018


Revised date: 2-10-2018
Accepted date: 2-10-2018

Please cite this article as: Athar H, Rehman Fazili Mu, Qayoom Mir A, Bashir
Gugjoo M, Ahmad RA, Khan HM, Ultrasonography: an affordable diagnostic tool
for precisely locating Coenurosis cyst in sheep and goats, Small Ruminant Research
(2018), https://doi.org/10.1016/j.smallrumres.2018.10.002

This is a PDF file of an unedited manuscript that has been accepted for publication.
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apply to the journal pertain.
Ultrasonography: an affordable diagnostic tool for precisely locating Coenurosis cyst in

sheep and goats

1
Hakim Athar, 2*Mujeeb ur Rehman Fazili, 3Abdul Qayoom Mir, 2Mudasir Bashir Gugjoo,

T
2
Raja Aijaz Ahmad, 3Hilal Musadiq Khan.

R IP
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1
Division of Veterinary Surgery and Radiology
2

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Division of Veterinary Clinical Complex
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3
Mountain Research Centre for Sheep and Goats
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Faculty of Veterinary Sciences and Animal Husbandry Sher-e-Kashmir University of
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Agricultural Sciences and Technology of Kashmir, India.


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*
Corresponding Author: 78, HIG Colony, Bemina, Srinagar, Kashmir, India. Pin: 190018
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Highlights
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 Ultrasonography is an affordable diagnostic tool for Coenurosis in sheep and goats.

 It is useful in assessing number, dimension and depth of brain cyst.


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 It is helpful in surgical decision making.

 It may improve outcome of surgery.

1
Introduction:

Chronic Coenurosis (Gid, Sturdy) a fatal disease in small ruminants results in heavy

economic loss to the farmer’s. The loss of elite germplasm due to such maladies is also a

matter of serious concern in research farms. Although having a worldwide distribution, but its

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prevalence is comparatively more in the developing countries (Shiferaw and Abdela, 2016).

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Most of the sheep rearing Indian states have reported the occurrence of Coenurosis in their

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animals (Godara et al. 2011; Sharma et al. 1998; Shivasharanappa et al. 2017; Soundarajan et

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al. 2017).

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Invasion of the larvae (metacestodes) called Coenurous cerebralis of Taenia
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multiceps (a tape worm that lives in the small intestine of dogs) is responsible for space-
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occupying cysts in the brain. Coenurosis is recognised in acute, quiescent or chronic forms
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(Gauci et al. 2008; Scala et al. 2007; Varcasia et al. 2009). The presumptive diagnosis of the

chronic disease depends on a careful neurological examination; changes in the general


ED

behaviour, postural aberrations and visual deficits (Gazioglu et al 2017). In order to ascertain

the specific location and the number of the cysts in an affected animal, additional reliable
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diagnostic tests are highly beneficial. Computed Tomography (CT) and Magnetic Resonance
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Imaging (MRI) are currently the techniques of choice (Gonzalo-Orden et al. 2000, Manunta
CC

et al. 2012). However, they are generally not affordable for use in farm animal practice.

Ultrasonography (USG) although bestowed with the inherent limitation for use over bones, is
A

comparatively very cheap and mostly available in university veterinary university hospitals

and the field polyclinics (Crilly et al. 2017). The veterinarians therefore try to utilize this

facility to explore even the less compatible organs including bones. In the available literature,

only two reports pertaining to the use of USG for the diagnosis of Gid in one lamb (Doherty,

2
1989) and four Jamunapari goats (Biswas, 2013) could be located traced. Both these

communications provide only a limited USG description of the USG findings cases.

Over last several years, the local stray dog population in and around this veterinary

faculty and its sheep and goat farm has shown significant and continuous increase.

Consequently, many sheep and goats with symptoms typical of chronic Coenurosis are

presented at Division of Veterinary Clinical Complex (University Referral Veterinary

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Hospital) for confirmatory diagnosis and treatment with symptoms typical of chronic

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Coenurosis. In this short communication, we wish to describe the USG findings of the brain

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cysts in such animals.

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Materials and methods:

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Animals: Sheep and goats (showing progressive central nervous system symptoms)
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belonging to the university farm (Mountain Research Centre on Sheep & Goats - MRCSG)
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showing signs involvement were presented for confirmatory diagnosis and treatment were
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included in this study. During a period of six months (November 2016 to April 2017), 12

animals (nine sheep and three goats), seven female and five male, aged 8-11(mean 10)
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months were all included in the study (Table 1).


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Clinical Examination: The routine preliminary clinical examination was followed by

detailed neurological examination evaluation with special attention to the general behaviour
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and the visuals deficits. Postural tests were also conducted for localization of the lesion.
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Palpation of the frontal area: Palpation of the frontal area was done using firm digital
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pressure meticulously to identify soft area/s of rarefaction in the underlying bone. The

rarefactions were graded as 0 to 2: 0 - no softening, 1- slight dimpling, 2- dimpling with

slight pressure. Palpations of the skull in all the animals were done by a single person.

3
USG scanning procedure: The hair over the fronto-parietal region was clipped and shaved

carefully. The ultrasound jelly was then applied liberally to the area. and scanning was

performed using 10-18MHz linear transducer (Esoate My Lab 40). The probe was initially

placed directly over the area of rarefaction in a transverse plane and then angled rostrally and

caudally. It was subsequently moved over the surrounding areas in caudo-rostral as well as in

and latero-lateral directions. In animals where softening was not detected on digital palpation,

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whole of the frontal area was scanned. The cysts were removed following the conventional

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surgical technique in all the animals diagnosed with Coenurosis.

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Results

History and Clinical Examination:

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The animals were presented with a history of progressive nervous signs varying from
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simple head tilt to complete recumbency. The clinical signs included head -pressing/-tilt/-held
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high, circling, somnolence, seizures, nystagmus, unilateral or bilateral blindness, partial or

complete anorexia, aimless walking or paddling, ataxia, loss of body condition and weakness.
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Softening of frontal bone was detected on palpation in 11 (grade 1=4, grade 2=7) animals.

One of the sheep showed two softened bone areas 2.0cm away from one another.
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Ultrasonographic findings:
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Eleven of the 12 animals were successfully diagnosed positive for Coenurosis by


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using ultrasonography (Table 2). All of them were found to have had one cyst per animal
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only. The near and the far boundary walls of the cysts was were visible as hyperechoic lines.

In six animals they were separated by a column of anechoic fluid in six animals (Figure 1, 4).

In five animals, half of the circumference of the cyst wall was visible as an echoic arc (Figure

2). Small echogenic spots representing scolices were visible inside the cyst in two animals

4
(Figure 3). Mean (± s.e) diameter of the cysts was 2.96±0.3cm. The smallest and the largest

were 1.33cm and 4.50cm in diameter respectively (Figure 1, 4). The distance of the near wall

of the cyst from the scanned cranial surface ranged varied from 0.50cm to 1.34cm with a

mean (± s.e) value of 0.83 (±0.10) cm (Figure 5). All the cysts recovered on surgery were

thin walled, filled with transparent fluid and numerous protoscolices on the inside wall.

Discussion:

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All sheep and goats included in this study were all less than one year old. Chronic

Coenurosis most frequently occurs in animals of more than 6 months age, the period required

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for cyst formation development and slow creation of local lesion development in the

cerebrum, cerebellum and spinal cord (Abera et al. 2016). According to Abera et al (2016),

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the animals with age of one to two years are more susceptible. Older sheep may develop
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acquired immunity (Gicik et al. 2007).
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Coenuruses is quite common in sheep and goats (Abera et al. 2016). In this study, the
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sheep outnumbered the goats. The low population of goats in the area and their preferred
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prehensile behaviour of browsing than close-grazing may be related to their comparatively

less prevalence involvement.


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The female animals in this study were more in number than the males. All the five
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animals included whose USG findings were described in the previous two studies reports
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were females only (Doherty, 1989; Biswas, 2013).

The clinical symptoms of chronic Coenurosis noticed in the animals included in this
A

study were same as similar to those reported earlier by several earlier workers (Sharma et al.

1989; Gicik et al. 2007; Scott 2012; Biswas 2013; Gazioglu et al. 2017). Although in most of

such cases, the show typical symptoms are typical yet diseases like listeriosis, louping-ill,

sarcocystosis, polioencephalomalacia and brain abscesses need to be ruled out (Scott 2012).

5
Successful surgical intervention depends on the precise localization of the brain cysts.

In most (80%-90%) of the animals, the cysts are located in one cerebral hemisphere. In 5%-

10% of the cases animals, they are found localize in the cerebellum (Scott 2012).

Normally, the brain is not accessible to ultrasonographic examination, as it is encased

in the skull. In chronic Coenurosis, the increased intracranial pressure due to by the growing

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cyst not only compresses the adjacent brain tissue causing specific clinical symptoms. but

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also It simultaneously pushes the overlying bone leading to its progressive softening

(rarefication). Thinning of the frontal bone segment provides a window for USG scanning

R
SC
(Scott 2012). In a few cases the bone rarefication has been detected some distance from the

area overlying the cyst (Scott 2012).

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Crilly et al (2017) used 6.0MHz sector transducer to identify Coenurosis cysts as
N
hypoechoic structures with acoustic enhancement at the distal edge. In our study, a linear 10-
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18MHz transducer provided better visualization (hyperechoic wall around anechoic fluid) of
M

the brain cysts. The distal acoustic enhancement was not detected in any of these animals

included in this study. However, inside two of them the scoleces were also detected.
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Ultrasonographic examination revealed varying distance of the cysts from the cranial

surface. The surgical intervention to locate and remove the deep cysts located deeply and
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those showing bone softening not directly over the cyst may pose problems for the surgeon,
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inadvertent trauma to the delicate nervous tissues of the animal and therefore unsatisfactory
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outcome. USG may therefore also help in arriving at the prognosis of the case and is

therefore thus recommended prior to the surgical intervention.


A

In animals with no skull softening, the position of the cyst can be determined during

neurological examination (Biswas 2013) but accuracy between clinicians varies from 54% to

81% (Skeritt and Stallbaumer, 1984). In our study one animal with no appreciable softening

6
was also found to have cerebral cyst on USG. Thus USG may also be helpful in detect cases

with initial stages of bone softening.

In another sheep bone softening was evident, but the cyst could not be visualized on

USG. In this animal, cyst was found in a deep location on postmortem examination. Doherty

(1989) failed to diagnose brain cyst in one lamb on USG preoperatively but could specifically

localize it intra-operatively. Removal of thin walled cysts filled with transparent fluid and

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scolices intraoperatively or on postmortem remain the definitive diagnosis of Coenurosis

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(Afonso et al. 2011). All the Coenurus cysts contain rose thorn protoscolices typical for

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Taenia multiceps (Rahsan et al. 2018).

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.In the present study, ultrasonography made possible the preoperative visualization of

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the coenurus cysts in most of the animals. The dimensions of the cysts and their distance
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from the skull surface could also be assessed. Previous USG reports pertaining to the small
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ruminants with Coenurosis have not described such the details (Doherty, 1989; Biswas,
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2013). Our observations support the statement of Doherty (1989) that the USG may not only

help a veterinarian to decide whether surgery in a particular animal would be feasible or not
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but also could improve the outcome of the surgery.

Conclusions:
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From this study, it is concluded that ultrasonography is an affordable, easy and


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efficient diagnostic tool for chronic Coenurosis in sheep and goats. Preoperative localisation
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of the cyst with precision and assessment of their it’s dimensions and distance from the skull
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surface may improve outcome of the surgery by minimising the intraoperative damage to the

brain. USG findings may also help in surgical decision making; deciding whether surgery

would be feasible or not.

7
CONFLICT OF INTERESTS

None

References

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Abera, S., Wubit, T., Abdela N. 2016. Cerebral Coenurosis in small ruminants: A review. J.

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Anim. Sci. Adv. 6: 1595- 1608.

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Afonso, S.M., Mukaratirwa, S., Hajovska, K., Capece, B.P., Cristofol, C., Arboix, M., Neves,
L. 2011. Prevalence and morphological characteristics of Taenia multiceps cysts

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(Coenurus cerebralis) from abattoir-slaughtered and experimentally infected goats.
Neuroparasitol. 2: 1-5.

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Biswas, D. 2013. Ultrasound diagnosis and surgical treatment of coenurosis (Gid) in Bengal
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goat (Capra hircus) at Chittagong metropolitan area, Chittagong, Bangladesh. Sci. J.
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Vet. Adv. 2, 68-75.


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Crilly, J.P., Politis, A.N., Hamer, K. 2017. Use of ultrasonographic examination in sheep
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veterinary practice. Small Rumin. Res. 152, 166-173.

Doherty, M.L. 1989. Ultrasonography as an aid to Coenurus cerebralis cyst localisation in


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lamb. Vet. Rec. 124, 591.

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Anderson, G.A., Lightowlers, M.W. 2008. Vaccination with recombinant oncosphere


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antigens reduces the susceptibility of sheep to infection with Taenia multiceps. Int. J.
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Parasitol. 38, 1041-1050.

Gazioglu, A., Simsek, S., Kizil, O., Ceribasi, A.O., Kesik, H.K. and Ahmed, H. 2017.

Clinical, pathological and molecular evaluations and CT scan screening of coenurosis

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(Coenurus cerebralis) in sheep and calves. Revista Brasileira de Parasitologia

Veterinária, 26, 3-9.

Gicik, Y., Kara, M., Arsalan, M.O. 2007. Prevalence of Coenurus cerebralis in sheep in Kars

province, Turkey. Bull. Vet. Inst. Pulawy. 51: 379-382.

Godara, R., Borah, M. K., Sharma, R. L., Jangir B. L. 2011. Caprine coenurosis with special

reference to hepatic coenurosis. Comp. Clin. Path. 20, 277–280.

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Gonzalo-Orden, J.M., Altónaga, J.R., Díez, A., Gonzalo, J.M., Orden, M.A. 2000.

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Correlation between MRI, Computed Tomographic findings and clinical signs in a

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case of ovine coenurosis. Vet. Rec. 146, 352-353.

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Gicik Y, Kara M and Arslan M. 2007. Prevalence of Coenurus cerebralis in sheep in Kars

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province, Turkey. Bull. Vet. Inst. Pulawy. 51: 379-382.
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Manunta, M.L., Evangelisti, M.A., Burrai, G.P., Columbano, N., Ligios, C., Varcasia, A.,
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Scala, A., Sanna Passino, E. 2012. Magnetic resonance imaging of the brain and skull
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of sheep with cerebral coenurosis. Am. J. Vet. Res. 73:1913-8.

Rahsan, Y., Nihat, Y., Bestami, Y., Adnan, A., Nuran, A. 2018. Histopathological,
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immunohistochemical, and parasitological studies on pathogenesis of Coenurus

cerebralis in sheep. J. Vet. Res. 62, 35-41.


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Scala, A., Cancedda, G.M., Varcasia, A., Ligios, C., Garippa, G., Genchi, C. 2007. A survey
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of Taenia multiceps coenurosis in Sardinian sheep. Vet. Parasitol. 143, 294-298.


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organized goat farms. J. Vet. Parasitol. 12, 30-32.

Shiferaw, A., Abdela, N. 2016. Public health and economic significance cerebral coenurosis

in sheep and goat: a review. Acta Parasitol. Globalis 7, 54–65.

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Shivasharanappa, N., Sharma, N., Sharma, D. K., Pawaiya, R.S.,Vamadevan, B., Mishra,

A.K., Paul, S. 2017. Neuropathological lesions of clinical and sub clinical Coenurosis

(Coenurus cerebralis) in organized goat farms in India. Acta Parasitologica, 62(2),

482–487.

Skerritt, G.C., Stallbaumer, M.F. 1984. Diagnosis and treatment of coenuriasis (gid) in sheep.

Vet. Rec. 115: 399-403.

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Soundararajan, C., Sivakumar, T., Balachandran. C. 2017. Coenurus cerebralis and its

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pathology in an organized farm of Tamil Nadu. J. Parasit. Dis. 41(2), 510–513.

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Varcasia, A., Tosciri, G., Coccone, G.N., Pipia, A.P., Garippa, G., Scala, A., Damien, V.,

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Vural, G., Gauci, C.G., Lightowlers, M.W. 2009. Preliminary field trial of a vaccine

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against coenurosis caused by Taenia multiceps. Vet. Parasitol. 162, 285-289.
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Figure Captions

Figure 1 B-mode sonogram of a superficially located Coenurus cyst (3.24cm diameter) in a


sheep.

Figure 2 B-mode sonogram of Coenurus cyst in a sheep: 1/2 of the circumference of the wall
visible as an echogenic arc.

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Figure 3 B-mode sonogram of Coenurus cyst in a goat showing scoleces as white spots inside

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the cyst.

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Figure 4 B-mode sonogram of a Coenurus cyst (1.33cm diameter) in a sheep; the near and the

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far cyst walls appear as echogenic lines on either side of the anechoic fluid column.

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Figure 5 B-mode sonogram of a deep (0.89cm) seated Coenurus cyst in a sheep.
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A Fig 1

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12
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A Fig 2

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Table 1: Particulars of sheep and goats with chronic Coenurosis

Case Species Breed Sex Age Bone


No. (months) rarefaction
1 Ovine Corriedale Female 08 01

2 Caprine Bhakarwal Female 10 01

3 Ovine Crossbred Male 10 02

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4 Ovine Crossbred Female 10 01

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5 Ovine Cross bred Male 11 01

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6 Ovine Cross breed Female 11 01

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7 Ovine Bhakarwal Male 11 01

8 Ovine Bhakerwal Female


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09 01
N
9 Ovine Cross bred Female 10 NIL

10 Caprine Bhakerwal Male 11 01


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11 Caprine Nondescript Male 09 01


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12 Ovine Cross bred Female 10 01


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A

17
Table 2: Ultrasonographic characteristics of Coenurus cysts in sheep and goats

Case CYST
No. No. Diameter Depth (cm) from Characteristics
(cm) bone surface
01 01 4.00 1.20 (a)

02 01 3.28 0.50 (a)

03 01 - - (b)

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04 01 3.20 1.31 (c) & (d)

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05 01 1.33 1.34 (c)

06 01 1.34 0.89 (c)

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07 01 4.50 0.70 (c)

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08 01 3.24 0.50 (c)

09 01 2.80 0.50
U (a)
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10 01 3.20 0.63 (a)

11 01 2.61 0.73 (a) & (d)


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12 01 3.10 0.80 (a)


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Mean 01 2.96±0.3 0.83±0.10 -


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(a) Both near and far cyst walls visible as echogenic lines separated by anechoic cyst
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fluid.

(b) Cyst not visualized on USG.


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(c) Half of the circumference of the cyst wall visible as an echogenic arc surrounding

anechoic cyst fluid.


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(d) Scolices visible as echogenic spots inside the cyst.

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