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Israel Journal of Veterinary Medicine  Vol. 70 (2)  June 2015 Gökçe, G. 40
Te First Report of Seropositivity for Neospora caninum in Sheep
from Turkey
Gökçe, G.,
1
Mor, N.,
2
* Kırmızıgül, A.H.,
1
Bozukluhan, K.
1
and Erkılıç, E.E.
1
1
Department of Internal Diseases, Faculty of Veterinary Medicine, Kafkas University, TR-36100 Kars, Turkey.
2
Kars School of Health, Kafkas University, TR-36100 Kars, Turkey.
Tis study was presented in 18
th
the National Congress of Parasitology (29 September – 5 October 2013, Denizli, Turkey).
*
Corresponding Author: Dr. Neriman Mor, Kars School of Health, Kafkas University, TR-36100 Kars, Turkey. Tel: +90 474-225 12 65 /
+90-474-225 15 67, Fax: 90-474-225 12 65. Email: nery.man@hotmail.com
ABSTRACT
Tis study was aimed at determining the seroprevalence of Neospora caninum infection in sheep raised in
Kars province and its vicinity in Turkey. Tree-hundred-and-seventy-six sheep of varying ages and breeds,
which were randomly selected from 5 foci located in the Kars region (Kars central district, and the Arpaçay,
Kağızman, Selim and Susuz districts). Te serum sample of each animal was tested for the presence of
antibodies against N. caninum using the ELISA test. Te test results demonstrated that, out of the 376 sheep
included in the study, 8 (2.1%) were seropositive for antibodies against N. caninum. Te highest seropositivity
rate (8.9%) was detected in the central district of Kars province, while the second highest seropositivity rate
(1.4%) was determined in the Susuz district. No anti-Neospora caninum antibodies were detected in the serum
samples of the animals raised in the Arpaçay, Kağızman and Selim districts. Te seroprevalence of neosporosis
in sheep raised in the Kars region was determined to be 2.1%. Tis is the frst report of seropositivity for N.
caninum in sheep from the Kars region and Turkey.
Keywords: Neospora caninum; Seroprevalence; Sheep; Turkey; Kars
INTRODUCTION
Neospora caninum is a heteroxenous obligate intracellular
parasite (1, 2). Te defnitive hosts of N. caninum are the
dog, coyote and fox (3, 4). Te intermediate hosts of the
parasite are cattle, sheep, goats, deers, and horses. While
Neospora causes neurological disorders in dogs and horses,
it leads to abortions in cattle, sheep, goats and deers. Tree
infective forms exist in the life-cycle of N. caninum, namely,
the tachyzoites, the bradyzoites found with in the tissue
cysts, and the sporozoites found with in the oocysts (5). Te
defnitive host becomes infected by ingesting food and water
contaminated with sporulated oocysts, and dogs become
infected by ingesting the cysts in the muscle tissue of the
intermediate hosts or by ingesting food contaminated with
sporulated oocysts (3, 6, 7). Furthermore, aborted foetuses,
placentae and uterine waste are the most common sources
of infection for the defnitive hosts of the parasite (5, 8, 9).
N. caninum infections are diagnosed on the basis of clini-
cal fndings, pathological fndings and serological test results.
As the infection has a sub-chronic course in sheep and pres-
ents with clinical fndings resembling those of several other
diseases, the diagnosis of neosporosis in sheep is difcul. For
this reason, immunohistochemical methods (10), serological
tests (11-13) and molecular biological techniques are used
to diagnose the disease (14, 15). Among serological tests,
ELISA has found common use in serological analyses, as it
produces results within a short period of time (11, 16, 17).
Although there are many research reports related to infec-
Israel Journal of Veterinary Medicine  Vol. 70 (2)  June 2015 41 N. caninum in Sheep from Turkey
tions of cattle and dogs, there is limited knowledge on sheep
(18-23). In Turkey, studies were conducted on more cattle
(24-28), but there is limited knowledge on dogs (18, 25, 29),
goats (30-32), horses (33, 34) and wild boars (35). Tere is
a dearth of studies on the presence of sheep neosporosis.
Similarly there have been some serological studies (25, 27, 36)
about dogs and cattle neosporosis in the Kars region, however
there is little information about neosporosis in sheep. Te
aim of the study is determine seroprevelance in sheep with
neosporosis in Turkey in the Kars region.
MATERIALS AND METHODS
Study Site and Animal Material
Tis study was conducted between January and May in
2013, in Kars province and its vicinity, in Turkey. Te Kars
region, located in north-eastern Turkey (43.05° E and 40.
36° N), is mountainous and has a cold climate. In total, fve
foci were selected to represent the Kars region (Kars cen-
tral district, and the Arpaçay, Kağızman, Selim and Susuz
districts). Tree-hundred-and seventy-six sheep, varying
from six months to fve years of age and of the Akkaraman,
Morkaraman and Tuj breeds, which were randomly selected
from the 5 foci, constituted the material of the study. Tis
study was approved by the Animal Ethical Committee of
Mehmet Akif Ersoy University (30.04.2014/79).
Collection of Samples
Ten-ml blood samples were collected from the jugular vein
of each of the 376 sheep into sterile vacuum tubes. Te tubes
were identifed with unique protocol numbers and trans-
ported to the laboratory. Te blood samples collected from
the sheep were centrifuged at 3000 rpm for 10 minutes for
the extraction of serum. Te sera were transferred into 1.5-ml
plastic tubes, labelled for identifcation, and stored at -20 ºC
in a deep freezer, until being tested.
Enzyme-linked Immunosorbent Assay (ELISA)
A commercial ELISA kit (Che kit Neospora caninum
Antibody ELISA test kit, IDEXX Laboratories, Berne,
Switzerland) was used to detect the presence of anti-N.
caninum antibodies in the serum samples. Te ELISA test
was performed in accordance with the instructions of the
manufacturer of the kit. Te absorbance of the colour change,
resulting from the reaction, was read at a wave length of 450
nm using an automated ELISA reader (Molecular devices
SPECTRAmax PLUS-384, Sunnyvale, California, USA),
and the measured values were recorded.
Interpretation of the Test Results
Te test results were calculated as percentage (%) inhibition
values, using the formula below:
% Inhibition = [(Optic Density (OD) of the Sample–OD
of the Negative Control) / (OD of the Positive Control –
OD of the Negative Control) x 100].
According to the calculations made using this formula, if the
percentage inhibition value of the tested sample was <30%,
the result was considered to be negative. If the resulting in-
hibition varied between 30-39%, the result was considered
to be uncertain, and if the inhibition was found to be >40%,
the test result was considered to be positive.
Te statistical evaluation of the seropositivity rates deter-
mined for the sheep with respect to the diferent age groups,
breeds and study sites (foci) was made using the SPSS 10.1
statistical software package and with the chi-square (
χ
2
) test.
P values smaller than 0.05 (P<0.05) were considered to be
statistically signifcant.
RESULTS
Out of the 376 sheep tested by ELISA in the Kars region,
8 (2.13%) were determined to be seropositive for antibodies
against N. caninum. Te comparison of the 5 foci, where the
study was carried out, showed that the highest seropositiv-
ity rate was in the central district of Kars province (8.86%),
followed by the Susuz district (1.35%). No antibodies were
detected in the serum samples of the sheep raised in the
Arpaçay, Kağızman and Selim districts (Table 1). Diferences
between the seropositivity rates for N. caninum with respect
to the study sites were found to be statistically signifcant
(P<0.05).
When evaluated for the diferent age groups, the highest
seropositivity rate was detected in sheep aged 1 to 3 years
(2.60%) and the lowest seropositivity rate was determined in
sheep older than 3 years of age (0.96%), (Table 2).
When evaluated for the diferent sheep breeds, the
highest seropositivity rate was detected in the Tuj sheep
(8.86%), while seropositivity was not detected in any of the
Akkaraman sheep (Table 3). Te seropositivity rate of the Tuj
Research Articles
Israel Journal of Veterinary Medicine  Vol. 70 (2)  June 2015 Gökçe, G. 42
breed was signifcantly higher than that of the Morkaraman
and Akkaraman breeds (P<0.05).
DISCUSSION
Te sero-diagnosis of neosporosis in cattle, dogs, sheep, goats
and horses has been investigated in many countries across the
world. Research has also been carried out on neosporosis in
cattle, goats, horses, dogs and wild boars in diferent regions
of Turkey, including the Kars region (24-36). However, to
the authors’ knowledge, ovine neosporosis has not been
investigated before either in the Kars region or in any other
part of Turkey. Terefore, the present study is the frst report
of neosporosis in sheep from Turkey.
Many researchers have been carried out worldwide on
ovine neosporosis, and the study with the closest proximity
to Turkey was conducted in the Mosul province of Iraq and
demonstrated a seroprevalence of 12.2% for N. caninum in
sheep (37). Seropositivity for neosporosis in sheep popula-
tions was reported as 1.70% in Iran (23) and as 27.7% in
Pakistan (38). In a study conducted in Britain and Wales,
out of 660 sheep presenting with abortion, only 3 (0.45%)
were determined to be seropositive using the direct ELISA
method and immunofuorescence antibody test (IFAT), and
it was suggested that the exposure of sheep to N. caninum in
their natural environment occurred rarely (11). Seropositivity
rates in sheep were reported as 1.8% in the Rio Grande do
Norte region of Brazil, based on IFAT results (39) and as 3%
in the Humid Pampa region of Argentina (40). Furthermore,
seropositivity was determined to be 2% in Italy (41) and
0.62% in New Zealand (42). In the present study, only 8 out
of 376 sheep (2.13%) having been determined to be seroposi-
tive, is in parallel with the fndings of some literature reports,
but on the other hand indicates a seropositivity rate lower
than that reported in some other studies. Te diferences
observed between these studies were attributed to these re-
searches having been conducted in diferent countries, as well
as to the diferences in the type of serological test applied, the
numbers and breeds of the tested sheep, and the numbers of
the defnitive hosts, namely, the dogs.
When evaluated for the fve diferent foci, the highest se-
ropositivity rate was determined in the central district of Kars
province (8.86%), while no antibodies were detected in the
serum samples of the sheep raised in the Arpaçay, Kağızman
and Selim districts. Te diference observed between the study
foci for seropositivity was considered to arise from the possible
contamination of the grazing area or feed, or from the num-
ber of infected dogs roaming in the site. In previous research
conducted in the Kars region with an aim to determine the
seropositivity rates of cattle for N. caninum, seropositivity was
ascertained as 2% by Akça et al. (36) and as 7.2% by Mor and
Akça (25). Te seropositivity results obtained for sheep in the
present study are similar to those reported by Akça et al. (36)
and lower than those reported by Mor and Akça (25).
In a study carried out in cattle raised in the Kars region,
Akça et al. (36) determined that, the seropositivity rates
Table 1. Te seroprevalence of N. caninum in sheep with respect to
the diferent foci
Study Site
(Focus)
Number
of tested
animals
Number of
seropositive
animals
Number
of suspect
animals
Seropositivity
(%)
Kars Central
District
79 7 1 8,86
b
Arpaçay 70 0 0 0
Kağızman 72 0 0 0
Selim 81 0 0 0
Susuz 74 1 0 1.35
a
Total 376 8 1 2.13
a, b: Diferences between the study sites shown with diferent
superscripts are statistically signifcant (P<0.05).
Table 2. Te seroprevalence of N. caninum in sheep with respect to
the diferent age groups
Age Group
Number
of tested
animals
Number of
seropositive
animals
Number
of suspect
animals
Seropositivity
(%)
<1 118 3 1 2.54
1-3 154 4 0 2.60
3> 104 1 0 0.96
Total 376 8 1 2.13
P>0.05
Table 3. Te seroprevalence of N. caninum in sheep with respect to
the diferent breeds
Breed
Number
of tested
animals
Number of
seropositive
animals
Number
of suspect
animals
Seropositivity
(%)
Akkaraman 70 0 0 0
Morkaraman 227 1 0 0.44
a
Tuj 79 7 1 8.86
b
Total 376 8 1 2.13
a, b: Diferences between the breeds shown with diferent superscripts
are statistically signifcant (P<0.05).
Research Articles
Israel Journal of Veterinary Medicine  Vol. 70 (2)  June 2015 43 N. caninum in Sheep from Turkey
detected in cattle of the Simmental breed were higher than
the seropositivity rates detected in the local cattle breeds.
Similarly, in their research on the seroprevalence of N.
caninum in sheep and goats, Nasir et al. (38) demonstrated
that seropositivity rates were signifcantly higher in short
and thin-tailed sheep. Tese results suggest that, in some
animal breeds, neosporosis may occur at higher rates. In the
present study, 7 out of the 79 Tuj sheep (8.86%), and only
1 out of the 227 Morkaraman sheep (0.44%) were found to
be seropositive, while all of the 70 Akkaraman sheep were
confrmed to be seronegative for N. caninum. Accordingly,
the seropositivity rate of the Tuj sheep being signifcantly
higher than that of the other sheep breeds included in the
study suggests that the Tuj breed could be more susceptible
to neosporosis.
While some researchers have reported age to be infuential
on seroprevalence (21), some other researchers have indicated
age not to have such an efect (13, 30). Abo-Shehadaand
Abu-Shehada 2010 (43) suggested that seroprevalence in-
creases with age, owing to an increased rate of ingestion of
sporulated oocysts, as a result of the horizontal transmission
of the infection, with age. In the present study, the evaluation
made for the diferent age groups demonstrated the high-
est seropositivity rate to have occurred in 1-to 3-year-old
sheep, yet no statistically signifcant diference was observed
between the diferent age groups for seropositivity (P>0.05).
In conclusion, the seroprevalence of neosporosis in sheep
raised in the Kars region was determined to be 2.13%. Tis
result demonstrates, for the frst time, the presence of N.
caninum in sheep from the Kars region, and from Turkey, on
the basis of serological analysis. Further research is required
to determine the prevalence of N. caninum in Turkey in dif-
ferent regions of the country.
ACKNOWLEDGEMENTS
Tis study was fnancially supported by Kafkas University
Scientifc Research Projects Unit (Project number: 2013-
VF-66). Te authors declare that they have no conficts of
interest.
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Research Articles