Toxoplasmosis in Four Caprine Breeds A Future Risk of Zoonosis Ahmad and Tasawar

Ahmad and Tasawar J. Anim. Plant Sci. 26(2):2016
388
TOXOPLASMOSIS IN FOUR CAPRINE BREEDS: A FUTURE RISK OF ZOONOSIS
S. Ahmad1*
and Z. Tasawar1
1
Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan, Pakistan
*
Corresponding author e-mail: saghir7np@yahoo.com
ABSTRACT
The present study was carried out to evaluate the seroprevalence of anti-Toxoplasma antibodies in four caprines breeds
that are commonly reared in Cholistan desert, Rajan Pur and Rahim Yar Khan during the period between April 2011 and
March 2012. The objective of the present study was to ascertain the infection rates of toxoplasmosis in different caprine
breeds so that the disease resistant goat breeds could be recommended for rearing in the study area. Blood samples were
collected from 865 goats reared in 21 flocks as well as from some domestically reared goats. The samples were
examined through Latex Agglutination Test to assess T. gondii infection. The overall seroprevalence of T. gondii in
caprines was 29.13%. Out of total four breeds of goats the highest infection rates 33.33% were found in Beetal followed
in sequence by 30.98% in Nachi, 29.06% in Teddy and the lowest infection rates were found 21.02% in Dera Din Panah
(DDP) breed. Non significant (P-Value= 0.5231) differences were observed in the overall high rates of toxoplasmosis in
caprines. The uniform values of Toxoplasma infection in all the four caprine breeds might be associated with the reason
that goats are allowed to breed naturally in the mixed flocks.
Key words: Toxoplasmosis, Latex agglutination test, goats.
INTRODUCTION
Domestic goats (Capra hircus) play an
important role in the food chain and by and large a source
of revenue of the countryside population (Lebbie, 2004)
all over the world. The goats are vulnerable to a range of
threats posed by infectious diseases caused by various
parasites (Siddiki et al., 2010). Additionally, the parasitic
infections lead to the decline in productivity due to early
death in the embryonic life, mummification, abortion or
stillbirths (Edwards and Dubey, 2013) thus causing the
economic losses. These infections have become a serious
threat to livestock (Lashari and Tasawar, 2011). One of
these infectious diseases is toxoplasmosis caused by the
parasite Toxoplasma gondii (abbreviated as T. gondii). It
is widespread in its distribution and can be considered as
one of the most successful protozoan parasites (Doskaya
et al., 2006) that can cause severe infections in all the
mammalian species, including caprines (Dubey, 2009) as
well as dogs the world over (Jadoon et al., 2009). This
disease is deleterious in terms of both economy of a
country and health of its people (Kijlstra and Jongert,
2009). Approximately thirty three percent of animals and
the human population of the world has been estimated to
be infected with T. gondii at an average (Sensini, 2006)
while according to Cook et al. (2000), the infection of
toxoplasmosis prevails from 30 to 63% in the humans.
This infectious disease has been established as a potential
economic threat for goat farming business, particularly
due to abortion all over the world (Innes et al., 2009) and
grave food hazard for human (Kijlstra and Jongert, 2009).
Some authors are of the view that it the ignored disease
of poverty (Hotez, 2008) or, to be concise, toxoplasmosis
can be dubbed as the disease of “poor people”
particularly those living in the underdeveloped countries
such as Pakistan.
T. gondii is found in three morphologically
different strains which are named as tachyzoite,
bradyzoite, and sporozoite. The tachyzoites are active,
proliferative forms found to exist in groups biologically
called the clones), the bradyzoites exist as tissue cysts,
and the sporozoites are found in oocysts in the
environment either soil, water or air (Dubey, 1993). As T.
gondii is a heteroxenous parasite, it requires more than
one host to complete the life cycle (Fig. 1). The sexual or
asexual phase of its life cycle is completed in cats, the
definitive or primary hosts, both domestic and wild or
any other member of the felidae family (Boothroyd,
2009). The asexual phase of life cycle of T. gondii is not
dependent upon the sexual cycle (Su et al., 2003). After
the completion of sexual or asexual life cycle, felids shed
the oocysts which harbor the sporozoites (Petersen and
Schmidt, 2003). On ingestion of food contaminated with
oocysts, the sporozoites present in the oocysts get entry
into the gastrointestinal tract of secondary host (Fig. 1)
that may be any kind of warm blooded animal including
cattle, buffaloes, sheep, goats, mice, humans, and birds in
which the asexual period of the life cycle is completed
(Boothroyd, 2009).
The occurrence of toxoplasmosis varies with the
differences in climatic conditions (Dubey et al., 2004).
For example, toxoplasmosis is more frequent, chiefly in
warm and moist climates (Dubey et al., 2004) because
the oocysts of T. gondii exhibit higher endurance and
survival in the areas having warm and moist climate
conditions in contrast to those which possess cold and dry
The Journal of Animal & Plant Sciences, 26(2): 2016, Page: 388-394
ISSN: 1018-7081

389
ones (Van der Puije et al., 2000). Hypothesizing the
climate conducive for proliferation of T. gondii infection,
we chose the current study area that experiences a longer
summer starting from mid of March and ending in the
mid of October with the temperature rising up to 51°
C
leaving notable effects of stress on the flora and fauna of
the region (Ali et al., 2009). On the other hand, the
average rainfall in the study area is less than 10 inches
and the only source of drinking water is the meager
rainfall water accumulated in natural depressions locally
known as “Dhands” and/or according to Ali et al. (2009)
some man-made ponds, named as “Tobas” in which
water never lasts for the long period of time either due to
seepage or evaporative loss (Ali et al., 2009). Therefore,
the animals inhabiting this area are left with meager
vegetation to be used as food.
Owing to these reasons, the animals remain
under the constant stress of harsh climatic conditions that
perhaps facilitates the better survival of the parasite. In
present survey the caprine breeds, namely Beetal, Teddy,
DDP and Nachi were selected for assessment of
toxoplasmosis because of being phylogenetically close
relatives of one another, as has been revealed by their
mtDNA investigation (Sultana et al., 2003). The study
was also aimed to establish the range of toxoplasmosis
rates in different caprine breeds whereby the infection
resistant breeds could be suggested for rearing in the
study area so that the human health could be ensured and
the parasite may not prove as the future health hazard.
MATERIALS AND METHODS
Study Area and Sampling Localities Distribution: The
animals used for sampling were distributed in the
following quadrants of study area:
a) The Cholistan Region Localities: In this region the
sampling was carried out from Lesser and the Greater
Cholistan sand dunes spanned between the border of
India in the east and agricultural areas of Rahim Yar
Khan in the west; b) Agricultural Region Localities: In
Agricultural Region of District Rahim Yar Khan, the
sampling was performed from caprines reared between
the boundary of Rajan Pur district and the Lesser
Cholistan desert in the east; and c) Reverine Region
Localities: In this region the sampling localities were
distributed between Agricultural region of Rahim Yar
Khan and the eastern bank of river Indus.
Sample Size: A total of 865 blood samples were
collected from goats (Table 1).
Samples Collection: In this study, the random sampling
technique (Thrusfield, 2005) was performed during the
collection of blood samples from following four caprine
breeds that are commonly populated in the herds or
reared domestically:
i. Beetal (also called Aseel)
ii. Dera Din Panah (abbreviated as DDP)
iii. Nachi (named so on the basis of its dancing gait)
iv. Teddy (a nickname given due to its dwarf size)
Exclusion Criteria: Following caprines fell in the ambit
of exclusion criteria in the current study: a) Jamnapari
and Juttal caprine breeds that were found in very small
numbers. b) The goats that were suspected to suffer from
some other disease were also excluded from sampling.
Sera Preparation: The blood samples (3 to 5 ml)
collected from the jugular vein of each goat in vacuum
tubes without the addition of anticoagulants were allowed
for about one hour to coagulate and subsequently
centrifuged at 3000 RPM for 10-15 minute for separation
of serum from blood corpuscles. Sera were decanted in
properly labelled, hygienic serum cups and stored at -
20°C for analysis. These samples were ready for the
detection of specific immunoglobulin G (IgG) through
serological assay.
Serological Assay: The serological analyses of anti-
Toxoplasma antibodies in sera were performed by using
commercially available kits, “Toxoplasmosis Latex”
manufactured by “ANTEC DIAGNOSTIC PRODUCTS-
UK for 50 or 100 tests.
Seropositivity Reaction: When the drop of LAT reagent
is added and mixed serum with antibodies anti-
Toxoplasma, an antigen-antibody reaction occurs that can
be expressed as under:
LAT + Serum (antibodies) = Agglutinate
Reagent and Controls: The commercial kit,
“Toxoplasmosis Latex” for 50 or 100 tests that are
available contains the following contents:
a. Latex reagent (the suspension of polystyrene
particles sensitized/coated with Toxoplasma antigens
in buffer containing bovine serum albumin < 0.1 %
Na-azide.
b. Positive control (the positive control shows
agglutination when added to the serum).
c. Negative control (the negative control does not
show agglutination when added to the serum)
Serological Assay: During the serological assay, the
steps followed were as under:
Both, the reagents and serum were brought at the room
temperature prior to use. Sera were diluted 1:16 in 0.9%
NaCl solutions (0.1 ml of serum + 1.5 ml of 0.9% saline).
One drop (50ul) of diluted serum was placed onto the
black area of the slide. The latex reagent was mixed well
and one drop was added to each serum drop. Both drops
were mixed with the aid of a stirrer and the slide was
tilted. The presence or absence of agglutination was
observed within the period no longer than three minutes.

390
The positive sera indicated the milky Latex agglutinates,
while in negative sera no agglutination was noted.
Statistical Analysis: The statistical analysis of results
were carried out by using Chi-square test for qualitative
variables such as infection rates in sex and breed of goats
via Pearson’s test through SSPS version 20.
Results Interpretations: The results were interpreted as
follows: a) the positive 1:16 sera indicated the milky
Latex agglutinates and b) the negative sera showed no
agglutination.
RESULTS AND DISCUSSION
Seroprevalence of toxoplasmosis via Latex
Agglutination Test and other techniques has previously
been reported in various animal species by many authors
such as (Jittapalapong et al., 2007) in caprines,
(Chaudhary et al., 2006) in buffaloes and humans,
confirmed by PCR, (Jadoon et al., 2009) in dogs, (Yang
et al., 2013) and (Lashari and Tasawar, 2010) in sheep
and (Zewdu et al., 2013) in caprines. In the present
findings, the overall infection rates of toxoplasmosis
29.13% (252/865) as shown in Table 1 were in agreement
with 27.9% observed by Jittapalapong et al. (2007) in
Thai goats and 30.7% reported by Tzanidakis et al.
(2012) in caprines farmed in Greece. The findings
showed the prevalence values higher than 9.0% reported
by Xu et al. (2014) in China, but lower than 42%
recorded by Chikweto et al. (2011) in goats sampled from
various Caribbean Islands. These disparities in the T.
godii seroprevalence rates might be associated with the
differences in study methods adapted by different authors
(Yu et al., 2007) and ecological factors prevailing in
various study areas (Dubey et al., 2004).
Among different breeds, the highest infection
rates 33.33% (95/285) were found in Beetal followed in
order by 30.98% (66/213) in Nachi, 29.06% (50/213) in
Teddy and the lowest infection rates 21.02% (41/195)
were found in Dera Din Panah abbreviated as DDP
(Table 1). The current results revealed the non significant
(P-Value= 0.5231) (Table 1) dissimilarities in
seroprevalence of T. gondii between all the four caprine
breeds in disagreement with (Van der Puije et al., 2000).
The non significant difference in infection rates of anti-
Toxoplasma antibodies in different caprine breeds can be
attributed to the mixed farming which is one of the
potential determinants of uniform proliferation of T.
gondii infection (Ali et al., 2009).
In Beetal breed, the toxoplasmosis infection
rates were found 38.35% (28/73) higher in bucks than
31.60% (67/212) in nannies (Table 2). There was no
significant (P-Value= 0.7736; OR= 1.3466; CL= 0.7749,
2.3400) difference in the T. gondii prevalence rates in
male and female caprines of Beetal breed (Table 2)
consistent with findings of Xu et al. (2014) reporting non
significant values of infections in females (9.58%) and
males (8.48%). As Beetal bucks are commercially reared
as favorable meat animals in almost all the parts of
Pakistan and due to their handsome morphological
features such as being Roman nosed, long eared and
comparatively long tailed breed of caprines, these
animals are the most purchased at the event of Eidul
Azha festival (the annually celebrated religious rite of
Muslims when animals are slaughtered for Divine will)
and for general food consumption. The higher infection
in the Beetal breed of caprines implies the health hazards
for human through zoonotic transmission of parasite
(Dubey et al., 2005). The popularity of Beetal goat breed
is also evident from the fact that the Agricultural region
of current study area harbors the largest population of this
breed of caprines in herds as well as in the mixed farms
of live stock comprising cattle, buffaloes, sheep and
goats. The uniformly higher infection rates in male and
female Beetal breeds warrant the possibility of genital
transmission of toxoplasmosis (Lopes et al., 2013) in
study area in general and particularly in the agri-based
localities of Rahim Yar Khan region.
The overall infection rates in the Teddy caprine
breed were found 29.06% (Table 1) in close agreement
with toxoplasmosis rates in caprines 27.9% reported by
Jittapalapong et al. (2007) in Thailand while the infection
rates were higher than 19.7% reported by Zewdu et al.
(2013) in caprines populated in Ethiopia. The Teddy
bucks showed the overall 30.50% (18 /59) incidence rates
of toxoplasmosis higher than female Teddy goats
showing 28.31% (32/1133) positivity for T. gondii
infection (Table 2) consistent with (Van der Puije et al.,
2000; Ramzan et al., 2009). Nevertheless, the results
revealed non-significant differences (P-Value = 0.9930;
Odds Ratio= 1.1112; CL= 0.5580, 2.2128) between the
infection rates prevailing in male and female Teddy
caprines (Table 2). The higher values of toxoplasmosis
established the poor management techniques (Zewdu et
al., 2013) adapted by Teddy goat breeders. This is
pertinent to mention that present study was a de novo
investigation to ascertain Toxoplasma infection at breeds’
level in Teddy caprines populated in drought facing
Cholistan desert and floods inflicted Rajan Pur region.
The uniformity in incidence of toxoplasmosis in the
bucks and does can also be explained through the
evidence that the Teddy males are usually not made
wether (sterile) unlike the males of other caprine breeds
that are castrated in the early age to increase the body
size. Such practice, it is suspected, provides the free
hand to highly aphrodisiac Teddy bucks to have the
chance of settling their fellow females Teddies leading to
the genital transmission of toxoplasmosis (Salant et
al., 2013). The Teddy females being highly prolific might
be responsible for the vertical transmission of
Toxoplasma infection (Habibi et al., 2012)
transplacentally during the gestation and also to the

391
human after their freshening though milk. Apart from
this, the Teddy goat breed was found reared in the mixed
caprine herds suggesting the possible transmission of T.
gondii from the other breeds of goats in the horizontal
fashion (Lim et al., 2013).
The overall seroprevalence rates recorded in
DDP breed, so far not reported by any author, were
21.02% (Table 1). The gender wise statistical analysis
showed that the infection rates in DDP were 24.13% and
20.48% in DDP breed male and females correspondingly
(Table 2). The study results revealed non-significant (P-
Value= 0.9777; OR= 1.2352; CL= 0.4878, 3.1279)
(Table 2) seroprevalence differences in DDP bucks and
nannies in agreement with (Ntafis et al., 2007) who have
also reported the non significant differences in the rates
of Toxoplasma infections in females and male goats. The
findings of this study disagreed with (Van der Puije et al.,
2000) in Ghana establishing significantly higher
infections of toxoplasmosis in female caprines as
compared with male animals, probably, due to the
disparity in management strategies used for goat flocks in
the respective areas of both studies (Zewdu et al., 2013).
The equal rates of infection speak of the possible natural
inbreeding resulting in sexual transmission (Gilbert et al.,
2003) of toxoplasmosis in the DDP caprines due to less
care for this less costly breed. The seroprevalence of T.
gondii infection were less than the mean values, about
30% reported in the world over (Sensini, 2006) and the
infection rates found in the overall caprine population
sampled in the current investigations. An important
justification of the lower rates of toxoplasmosis in this
breed was the remoteness of its habitat in the Lesser
Cholistan and the Greater Cholistan sand dunes localities
with lesser access of cats than other regions of present
study area (Hove et al., 2005). The evenness in the
seroprevalence of T. gondii infection in DDP caprines
can be the source of the vertical (Lopes et al., 2013) as
well as horizontal transmission of disease (Asgari et al.,
2011) and impending zoonosis as well.
Out of total 213 Nachi breed of caprines
sampled, 66 (30.98%) were found seropositive for
infection of anti-Toxoplasma antibodies (Table 1). The
seroprevalence rates in female 32.21% (48/149) and male
animals 28.12% (18/ 64) were non-significant (P-Value=
0.9503; OR=0.8233; CL= 0.4325, 1.5673) (Table 2) in
disagreement with (Van der Puije et al., 2000) who have
reported significantly higher values of toxoplasmosis
infection in female goats as compared with males in
Ghana. The varied infection rates might be the outcome
of differential ecological factors prevailing in Ghana and
the current study area (Dubey et al., 2004). The
uniformly higher rates of toxoplasmosis infection can be
attributed to the sexual transmission of infection within
the animals (Lopes et al., 2013), substandard
management system (Zewdu et al., 2013) and careless
breeding of animals without screening of bucks and does
before mating thus providing the possible chance of
exchange of T. gondii tachyzoites’ infestation during
coitus. This suspicion about the sexual transmission is
evident from the fact that the seminal samples taken from
rams (Lopes et al., 2013) and canines (Arantes et al.,
2009) have been proven to be positive for Toxoplasma
strains.
The uniform values of toxoplasmosis observed
in all caprine breeds (Table 1) might be related with the
reason that goats are allowed to breed naturally, except
for the selection of morphologically sturdy bucks for the
whole herd which is a sort of limited artificial selection,
adapted by least number of farmers. Another aspect that
justifies the uniformly higher values of T. gondii
infection in caprines is the absolutely careless inter
breeding between different breeds of goats, as was
observed during the whole span of present investigation.
Possibly, the interbreeding must have facilitated the
parasite to make its way of dispersal in different breeds
through genital passages (Habibi et al., 2012). The
higher infection rates bring to the hypothesis that
zoonotic transmission (Dubey et al., 2005) of T. gondii
from caprines to human population might be taking place
in nearby urban and remote areas of Pakistan where these
animals are sold for human’s consumption.

392
Fig. 1: Life cycle and mode of transmission of Toxoplasma gondii
Conclusion: The seroprevalence of toxoplasmosis in the
caprine population of the study area recorded up to
29.13% demands the further study and application of
control measures to prevent the proliferation of
toxoplasmosis caused by parasite T. gondii. It was
seriously noted that the basic health facilities and
veterinarians in the study area were the insufficient. Thus
the goats and other livestock animals are, by large, left at
the mercy of parasitic infections. The gender wise
uniform rates of infections in goats warrant the horizontal
transmission of the disease in different caprine breeds
because the parasitic infections have no boundaries.
Recommendations: The little work has been done in the
study area to investigate T. gondii infection in the past,
particularly in the livestock animal species. As T. gondii
is transmitted to humans through zoonosis (Dubey et al.,
2005), it is warranted that the other species of meat
producing animals must also be screened for occurrence
of toxoplasmosis. Furthermore, mix farming of different
caprine breeds must be discouraged. It is recommended

393
that the DDP breed of caprines showing less prevalence
of toxoplasmosis is suggested for rearing in the study
area.
Keeping in view, the high rates of toxoplasmosis
in goats it is inferred that the T. gondii infection might be
occurring in the human population of the study area.
Therefore, it is also recommended that human population
residing in Cholistan, Rajan Pur and Rahim Yar Khan
Districts of Pakistan must also be screened for the
Toxoplasma infection in the public interest.
Acknowledgments: This study project was financially
supported by funds granted by the Higher Education
Commission (HEC), Islamabad, Pakistan under
Indigenous 5000 PhD Fellowship Program, Batch III, and
PIN: 063-161120-Bm3-093.
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