Seroprevalence of Toxoplasma gondii in Four Ovine Breeds of Cholistan Desert of Pakistan

Abstract

Seroprevalence of Toxoplasma (T.) gondii in four ovine breeds was carried out in
Cholistan desert and adjacent regions of Southern Punjab, Pakistan from May 2012
to April 2013 to compare the rates of infection in different ovine breeds so that the
infection resistant breeds could be recommended to the farmers of these regions.
The study was also aimed to evaluate the infection rates at gender level in all ovine
breeds to infer the vertical transmission of Toxoplasma infection. Serum samples
were collected from 20 spatially reared ovine herds and examined by Latex
Agglutination Test. Out of total sampled sera, 37% were found positive for anti-T.
gondii antibodies. At breeds level, the non significant differences in seroprevalence
rates were found as 45.09%, 44.18%, 39.68%, and 28.69% in Kajli, Thalli,
Cholistani and Lohi breeds, respectively. At gender level, the findings showed
varied trends of seroprevalence in male and female animals. Moreover, the results
established the overall high rates of seroprevalence of T. gondii in sheep that
warranted the threat of public health via zoonotic transmission of toxoplasmosis.

Full text

91
Pak.j.lifesoc.Sci.(2015),13(2):91‐96

E‐ISSN:2221‐7630;P‐ISSN:1727‐4915

PakistanJournalofLifeandSocialSciences
www.pjlss.edu.pk
RESEARCH ARTICLE
SeroprevalenceofToxoplasmagondiiinFourOvineBreedsofCholistan
DesertofPakistan
Saghir Ahmad* and Zahida Tasawar
Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan, Pakistan
A
RTICLE INFO
ABSTRACT
Received:
Accepted:
Online:
Dec 15, 2014
Aug 01, 2015
Aug 25, 2015
Seroprevalence of Toxoplasma (T.) gondii in four ovine breeds was carried out in
Cholistan desert and adjacent regions of Southern Punjab, Pakistan from May 2012
to April 2013 to compare the rates of infection in different ovine breeds so that the
infection resistant breeds could be recommended to the farmers of these regions.
The study was also aimed to evaluate the infection rates at gender level in all ovine
breeds to infer the vertical transmission of Toxoplasma infection. Serum samples
were collected from 20 spatially reared ovine herds and examined by Latex
Agglutination Test. Out of total sampled sera, 37% were found positive for anti-T.
g
ondii antibodies. At breeds level, the non significant differences in seroprevalence
rates were found as 45.09%, 44.18%, 39.68%, and 28.69% in Kajli, Thalli,
Cholistani and Lohi breeds, respectively. At gender level, the findings showed
varied trends of seroprevalence in male and female animals. Moreover, the results
established the overall high rates of seroprevalence of T. gondii in sheep that
warranted the threat of public health via zoonotic transmission of toxoplasmosis.
Keywords
Cholistan desert
Latex Agglutination Test
Sheep breeds
Toxoplasmosis
*Corresponding Author:
saghir7np@yahoo.com

INTRODUCTION
The domestic ovines (Ovis aries) are the source of milk
and meat particularly in the rural areas (Pugh, 2002).
Sheep milk is an outstanding unprocessed material for
the milk industry particularly in the manufacture of
cheese (Park et al., 2007). These small animals are
vulnerable to a wide range of infectious diseases (Bilal
et al., 2009) caused by various pathogens including
parasites (Ijaz et al., 2009) that pose menace to their
health and create limitations in their productivity
(Nwosu et al., 2007) due to early embryonic life death,
mummification, abortion, stillbirth or the adult
mortality (Panadero et al., 2010). One of the potential
infectious diseases faced by ovines species is
toxoplasmosis, caused by an apicomplexan parasite,
Toxoplasma (T.) gondii (Edwards and Dubey, 2013).
The infection of toxoplasmosis, whether acute or
chronic, can be recognized by detection of anti-T.
gondii IgG, IgM, IgA and/or IgE antibodies from
infected animals (Pignanelli, 2011) depending upon
different genetic types (strains) of T. gondii (Singh,
2003; Pignanelli, 2011). It is widely accepted that
Toxoplasma has a number of genetic types but about
95% of them are categorized into three classes of
strains simply named as Type I, II and III (Sibley,
2003). These genotypes are considered to be clonal in
their structural features (Dubey et al., 2010). Type I
causes infection in rodents. Type II has been
established as the infectious agent of toxoplasmosis in
small ruminants while Type III has yet not been proved
as infectious strain. All the three genetic types I, II and
III can cause toxoplasmosis in human (Boothroyd and
Grigg, 2002). Recently, a newly discovered genotype
(Type IV) has also been reported in some game animal
species (Khan et al., 2011). The infection of T. gondii is
more detrimental to humans as compared to other
mammalian species. The humans contact this parasite
mainly by consuming the infected edible items such as
mutton or beef carrying bradyzoites (Qiu et al., 2012),
water polluted with oocysts of T. gondii (Montoya and
Liesenfeld, 2004) or by intake of unpasteurized milk
(Higa et al., 2010). On infecting the human body, T.
gondii causes not only abortion and reproductive issues
in women (Dubey, 2009) but also a variety of diseases
in both men and women such as schizophrenia (Flegr,
2013), ocular infection and encephalitis (Boothroyd and
Grigg, 2002).
No study has been reported on this disease in ovines
breeds of Cholistan area of Pakistan. Nevertheless, the
sheep reared in nearby area of Rahim Yar Khan were
reported by Ramzan et al. (2009) for the infection of T.

Ahmad and Tasawar
92
gondii. As Cholistan desert is the far reached and the
most neglected area in connection with the study of
toxoplasmosis due to lack of infra structure, it was
hypothesized that the parasite might be multiplying
vertically (Lopes et al., 2013a) due the little attention by
the authorities leading to the serious consequences of
zoonosis (Stormoen et al., 2012) with the passage of
time. Moreover, the disease might be causing harms to
the economy of people. It is anticipated that the present
study would enable the authorities to save the human
from economic losses as well as imminent zoonosis.
Furthermore, the study would also provide an insight to
the livestock farmers for rearing the disease resistant
breeds of sheep in the study area.
MATERIALS AND METHODS
Blood samples (n=335) were collected from four
different sheep breeds viz Kajli, Thalli, Cholistani and
Lohi for detection of anti-T. gondii antibodies. Three to
five ml of blood was collected from the jugular vein of
each animal in a vacutainer and allowed for about 1
hour to coagulate. Sera were isolated by centrifugation
(3000 rpm) for 15 minutes and examined for detection
of anti-T. antibodies (IgG) by Latex Agglutination Test
using commercially available kits, “Toxoplasmosis
Latex” manufactured by “ANTEC DIAGNOSTIC
PRODUCTS-UK. The results were statistically
analyzed by applying Chi-square test for evaluation of
infection rates in male and female sheep as well as in
the selected breed of sheep via Pearson’s test through
SSPS version 20.
RESULTS
The overall seroprevalence in all the sampled ovine
breeds was 37.31% (n=125/335). The seroprevalence
rates of anti-T. gondii antibodies were 30% and 66.66%
in males and females of Kajli sheep breed, respectively.
In Thalli breeds, seroprevalence rates were 46.66% and
42.85% in males and females, respectively. The
seroprevalence rates of anti-T. gondii antibodies in rams
of Cholistani (also called Buchi) breed were 30.95%
while infected ewes were 44.04%. On the other hand,
these seroprevalence rates were 28.04% and 30.30% in
males and females of Lohi breed of sheep (also called
Parkanni), respectively.
DISCUSSION
In the present study, four selected ovine breeds namely
Kajli, Thalli, Cholistani and Lohi with varied
populations in the study area were investigated. The
overall seroprevalence rate of anti-T. gondii antibodies
in sheep breeds was 37.31% (Table 1) that was in
agreement with several previous studies such as 37% in
Table 1: Seroprevalence of Toxoplasma gondii in four
breeds of sheep
Sheep breed No. of sheep
examined No. of sheep
infected Prevalence
(%)
Cholistani 126 50 39.68
Kajli 51 23 45.09
Lohi 115 33 28.69
Thalli 43 19 44.18
Total 335 125 37.31 *
Chi-Square = 2.863, P-Value = 0.413, *P<0.05
Egyptian sheep (Shaapan et al., 2008), 37.5% in Iranian
ovines (Asgari et al., 2011) and 36.0% in ovines of
Khyber Pakhtoon Khawah (Shah et al., 2013).
Contrary to this, current findings also indicated higher
seroprevalence rate as compared to some previous
studies conducted in different parts of the world
(Ramzan et al., 2009; Yang et al., 2013; Lopes et al.,
2013b; Cenci-Goga et al., 2013) and lower than
seroprevalence rate reported in Brazilian population of
sheep (57%) (Tembue et al., 2009). The deviations in
the seroprevalence rates can be attributed to differences
of resistance to parasitic infection in different ovine
breeds included in the present study and those
examined in other parts of the world. The varied rates
of toxoplasmosis might be the outcome of varied
serological techniques used in different regions of the
world. Furthermore, different geo-climatic conditions
might also be speculated as one of the possible reasons
behind varied seroprevalence rates of toxoplasmosis in
different regions of the world (Chacin-Bonilla and
Sanchez-Chavez, 2000; Tenter et al., 2000; Kniel et al.,
2002; Hill et al., 2005).
Results of present study revealed varied rates of
seroprevalence of toxoplasmosis in different sheep
breeds (Table 1). The highest anti-T. gondii antibodies
prevalence rates were observed in Kajli breed (45.09%)
followed by Thalli (44.18%), Cholistani (39.68%) and
Lohi (28.69%), respectively. Although the
seroprevalence rates ranged from 28.69% to 45.09% in
all the four breeds yet differed non-significantly (P-
value= 0.523) (Table 1). This trend of non significant
differences in seroprevalence rates was coincident with
31.1% and 43.2% evaluated through ELISA and IFAT
correspondingly by Carneiro et al. (2009) in Brazil.
However, the results showed a disagreement with
findings of Lashari and Tasawar (2010) who studied
Lohi and Kacchi breeds of sheep and found the
significantly (P<0.05) different rates of seroprevalence
of toxoplasmosis in the two selected breeds. Further,
the seroprevalence rate in Lohi breed was higher than
that reported in an earlier study 15% (Lashari and
Tasawar, 2010). The lowest rates in Lohi breed of
sheep can be associated with the popularity of this
ovine breed (Ahmad et al., 2001) earning more
attention of the farmers with commercial point of view
and being good performer in terms of meat and milk

Seroprevalence of Toxoplasma gondii in ovine breeds 
93
Table 2: Toxoplasmosis in different ovine breeds at gender level
Sheep
breed Sex No. of sheep
examined No. of sheep
infected Prevalence
(%) Chi-Square P-Value OR CL
Kajli
Male 30 9 30
6.708 0.010 0.2142 0.667-0.6875
Female 21 14 66.66
Thalli Male 15 7 43
0.057 0.811 1.1666 0.3291-4.1357
Female 28 12 19
Cholistani Male 42 13 30.95
163.9929 0.000 0.6956 0.6580-0.7353
Female 84 37 44.04
Lohi Male 82 23 28.04
0.699 0.403 1.4523 0.6054-3.4837
Female 33 10 30.30
OR= Odd’s Ratio, CL=Confidence Limits
production earning the highest exchequer for the
farmers. The Cholistani sheep are reared most
commonly in desert region where the persistent stress
caused by scarcity of food and water is faced by
animals. Owing to the unrelenting stress conditions, the
susceptibility to parasitic infections by these animals
might be higher (Khan, 2006). One of the vital factors
rendering the animals more vulnerable to infections was
the closed housing in the area of study as is evident
from a previous study reported by Sajid et al. (2012).
Amongst the variety of determinants accounted for the
higher prevalence of infections in all the four breeds of
sheep, the most considerable one was the interbreeding
in different breeds of sheep without screening of the
breeding rams for pathogenic organisms. This
proliferation of infection might be taking place due to
mixed farming of different breeds (Ali et al., 2009) as is
in vogue in the current study area.
At gender level, Kajli males 30% (n=9/30) showed
significantly lower (P-Value= 0.010; OR= 0.214; CL=
0.0667, 0.6875) seropositive rate for ant-T. gondii
antibodies as compared to female Kajli sheep (66.66%)
(Table 2). Significantly higher prevalence rate in Kajli
ewes as compared to rams was in a disagreement with
Tasawar et al. (2011) who reported higher prevalence in
rams than in ewes. These differences in the findings
might be due to differential techniques in both studies.
Lower rates of toxoplasmosis in rams as compared with
the ewes can be attributed to the differential feeding
practiced for both genders. The Kajli rams with
beautiful eyes, curved nose and attractive stature are
considered as financial darlings. These are perhaps the
most costly rams in Pakistan and thus are usually fed at
pens with concentrate fodder while the ewes are
nourished through pasture grazing that probably renders
them more vulnerable to the ingestion of oocysts from
environment (Gangneux and Darde, 2012).
Contrary to Kajli breed, males of Thalli breed showed
higher seropositivity for anti-T. gondii antibodies as
compared to females but difference was statistically
non-significant (P-value= 0.811; OR= 1.166; CL=
0.3291, 4.1357). This finding was in line with many
previous studies on ovine toxoplasmosis (Williams et
al., 2005; Ntafis et al., 2007; Carneiro et al., 2009). The
analogous non-significant results were also reported in
ovine population of China by Wanga et al. (2011).
Further, these findings were also in disagreement with
some previous studies (Asgari et al., 2011; Abu-
Dalbouh et al., 2012). The non significant variation in
occurrence of toxoplasmosis at gender level in Thalli
breed of ovines was possibly due to the exchange of
infection by male and female animals, during natural
mating, primarily infected from the contemporary
breeds of ovines (Tenter et al., 2000; Lopes et al.,
2013a) or environment including soil and water polluted
with oocysts of T. gondii (Al-Jebouri et al., 2013). It is
noteworthy that Thalli sheep is reared by poor
communities of farmers depending almost totally upon
pasture feeding, a well known cause of higher
toxoplasmosis in animals due to T. gondii oocysts conta-
mination (Kniel et al., 2002; Al-Jebouri et al., 2013).
In Cholistani breed, overall seroprevalence rate was
39.68%, whereas, at gender level, females showed
significantly higher (P=0.029) rates as compared to
males. These findings were consistent with the results
of overall previous study on ovine populations of
Rahim Yar Khan (Ramzan et al., 2009) and in another
study on mixed breeds of ovines reported by Lashari
and Tasawar (2010) from Multan region. The overall
higher seroprevalence of anti-T. gondii antibodies in
Cholistani ovine breed might be the outcome of lack of
health facilities available for animals (Farooq et al.,
2012), crude management techniques and prototype
subsistence farming in the Cholistan region. The
animals consume a bulk of stored energy to access the
sources of water called Dhands which are only seasonal
lakes (Ahmad and Tasawar, 2015) thus being more
exposed to parasitic infection due to attenuated physical
conditions and consequently the poor immunity level.
Lohi breed showed higher rates of seropositivity for T.
gondii in females as compared to males but the
difference was non-significant (P-Value= 0.403; OR=
1.452; CL= 0.6054, 3.4837) and was in consistence
with findings of Carneiro et al. (2009) who reported
non-significant relationship between genders of ovines
and toxoplasmosis. Similar non-significant values of T.
gondii infections were reported by Williams et al.
(2005) and Ntafis et al. (2007) in ovines.

Ahmad and Tasawar
94
The higher incidence of toxoplasmosis is facilitated by
the persistent stress inflicted by lack of natural foliage,
the only fodder source and water as well in the most
part of the year. Additionally, the dhands in this region
provide an ephemeral stay to the Russian migratory
avian species that follow the Indus fly way during their
nuptial flight towards Manchar lack, Keenjhar lack and
Kalari lack in Pakistan. It is also suspected that the
Cholistani mammalian species together with Cholistani
ovine breeds must share the infection left by the
migratory birds (Cabezon et al., 2011) via felines
(Boothroyd, 2009).
Conclusions and recommendations
The seroprevalence of T. gondii in the ovine population
reared in different localities of Cholistan desert was
considerably high that demands further investigations
and application of control measures to avoid the
proliferation of toxoplasmosis. Lohi and Cholistani
(buchi) breeds have been found comparatively more
resistant to toxoplasmosis in the study area. Therefore
these two breeds are recommended for rearing in
Cholistan. Moreover, mixed farming is in vogue in
Cholistan, the screening of animals of other species of
the study area is recommended to evaluate the
prevalence of T. gondii infection transmitted via
horizontal fashion. At butcheries, the leftover meat of
enormous number of T. gondii infected animals reaches
the intestinal tract of cats which add the oocysts in the
environment leading to the infestation of populations of
same species through a sort of theoretical ‘positive
feedback infestation’. Therefore, it is recommended that
along with the other measures, the stray cats’ study
evaluating the infestation status must be conducted in
the study area.
Acknowledgements
The authors are thankful to Higher Education
Commission (HEC), Islamabad, Pakistan for provision
of funds to meet the financial needs during the current
project under Indigenous 5000 PhD Fellowship
Program, Batch III (PIN: 063-161120-Bm3-093). The
authors are indebted to pay thanks to the ovine farmers
who allowed collecting the blood samples from their
animals.
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