Seroprevalence and spatial distribution
Results revealed an overall seropostivity as 40.58% (n=334) for
T. gondii antibodies in small ruminants in Punjab state. Spatial distribution of data showed highest prevalence in district Barnala (54.80%) and lowest in S.B.S. Nagar (11.76%) (Table 1, Fig 1). Species wise highest seroprevalence for
T. gondii in goats and sheep was seen in districts Sangrur (58.49%) (Table 1, Fig 2) and Fazilka (100%) (Table 1, Fig 3) respectively.
Zone-wise highest seroprevalence was recorded in Zone IV (45.78%) followed by Zone III (41.14%), Zone V (39.18%), Zone II (32.40%) and lowest in Zone I (25.00%) (Table 2, Fig 4). Predictive seroprevalence of toxoplasmosis at un-sampled locations based on the spatial distribution indicated small ruminant population in the districts adjoining Haryana and Rajasthan states at more risk, while animals of districts adjoining to the Himalayan region are at lower risk of toxoplasmosis (Fig 5, 6 and 7).
The present study, a first systematic report on spatial seroepidemiology of toxoplasmosis with overall seroprevalence of 40.58%, indicated wide exposure of small ruminants to
T. gondii in Punjab. However, previous single study on seroprevalence of toxoplasmosis in 186 sheep examined from Punjab, showed low level of antibodies of
T. gondii (
Sharma et al., 2008). High seroprevalence of
T. gondii in small ruminants from adjoining Punjab province of Pakistan
(Ahmad et al., 2015) is indicative of similar geoclimatic conditions in both neighboring nations. High seroprevalence in sheep and goats, indicated that the meat-producing animals may be a great threat to human population if their meat is consumed undercooked. Further, there is possibility of economic losses to farmers as toxoplasmosis is responsible for abortion, stillbirth and neonatal mortality in sheep and goats
(Dubey et al., 2011).
Associated risk factors
Sheep were at apparently higher risk of
T. gondii infection (OR=1.14, 95% CI: 0.84-1.54, P=0.431) as compared to goats (OR=0.87, 95% CI: 0.63-1.19, P=0.431) with an overall seropositivity in sheep 42.85% and 39.60% in goats (Table 2). Among zones (I toV) seroprevalence ranged from 25-45.78%, being non significantly highest in zone IV.
Apparently higher seropostivity in goats of > 1 year (39.70%) (OR=1.02, CI=0.65-1.59, P=0.92) was seen as compared to < 1 year of age (OR=0.97, Cl=0.62-1.52, P=0.92). Similarly in sheep animals > 1 year of age were apparently at more risk to toxoplasmosis (OR=1.01, CI=0.57-2.10, P=0.70) as compared to animals < 1 year of age (OR=0.90, Cl=0.46-1.76, P=0.70).
Risk factor analysis indicated that goats with history of abortion were 1.72 times (OR=1.72, CI=1.15-2.56, P=0.008) and sheep were 2.74 times (OR=2.74, CI=1.31-5.71, P=0.006) more at risk to
T. gondii as compared to animals with no history of abortion. The seropostivity in goats from farms having frequent access to cats was high (41.40%) to toxoplasmosis as compared to farms having limited access (25.00%) revealing 2.03 times more at risk (OR=2.03, CI=1.05-3.90, P=0.03). Similarly, in sheep higher seropostivity was observed in animals with frequent cat access (48.01%) and were 4 times more at risk to toxoplasmosis (OR=4.04, CI=1.78-9.14, P=0.01) as compared to animals belonging to farm with limited cat access.
Goats with history of grazing only, were 1.65 times higher (OR=1.65, CI=0.87-3.16, P=0.12) at risk to
T. gondii infection (40.56%) as compared to animals with grazing coupled with stall feeding (29.16%). Similar pattern of seropositivity in sheep (43.77%) with history of only grazing found 1.40 times (OR=1.40, CI=0.62-3.18, P=0.42) at higher risk of toxoplasmosis as compared to other animals with grazing coupled with stall feeding (35.71%). Gender-wise more seroprevalence was observed in females in both goats (40.03%) and sheep (43.50%) as compared to males as none of the animal was found seropositive.
As in the present study sheep being more susceptible to disease as compared to goats, previous studies from Brazil
(Pinheiro et al., 2009), Egypt
(Ghazi et al., 2006) and Pakistan
(Ahmed et al., 2016) also indicated sheep at higher risk of toxoplasmosis. It might be due to the fact that samples from sheep were collected from grazing system, while some of sampled goats were reared in the intensive system. Overall higher seroprevalence in sheep could be due to the possibility of picking up infective oocysts from ground as compared to goats as sheep is a ground grazer and goats are browser. On the contrary,
Ahmed et al., (2016) reported higher infection rate in goats as compared to sheep.
Higher seroprevalence in Zone III, IV and V adjoining to Rajasthan and Haryana states as compared to Zone I and II adjoining to Himachal Pradesh may be related to higher temperature, lower precipitation and lower altitude compared to the absence of
T. gondii at other locations
(Kantzoura et al., 2013). Previous workers reported the toxoplasmosis is more prevalent in humid and damp areas than in dry and hot environmental conditions (
Dubey and Thulliez, 1993,
Singh and Nautiyal, 1991). It was observed that majority of small ruminant farmers in Zones III-V, were nomads, while majority of animal owners of Zones I and II reared their animals in fixed position due to availability of ample fodder. One possible reason for more seroprevalence in zones 3, 4 and 5 could be the more movement of animals in these zones and more sale and purchase of animals with adjoining states Haryana and Rajasthan. An increased in the
T. gondii antibodies level with higher age in both sheep and goats could be possible as older animals are more exposed to pathogens than the younger ones
(Li et al., 2016; Othman and Al-Azuheir, 2014;
Puije et al., 2000). Previously similar observations were reported by
Lashari and Tasawar (2010);
Tasawar et al., (2011) and
Ramzan et al., (2009).
Significantly higher sero-prevalence observed in animals having history of abortion indicates that
T. gondii could be an important abortifacient agent in small ruminants.
Presence and frequent access of cats to small ruminant farms as a significant risk factor for higher seroprevalence may be due to fact that cats being the definitive hosts of the parasite play a vital role in infecting intermediate hosts by shedding oocysts in the environment
(Lopes et al., 2010). One study from Poland revealed the presence of free-roaming cats as important risk factor for the transmission of toxoplasmosis in goats
(Neto et al., 2008).
More seroprevalence observed in animals reared on grazing system corroborates with the published reports on the assessment of different type of feeding practice revealing animals being raised extensive system to be more prone to the infection
(Lopes et al., 2010; Wang et al., 2011).
Higher seroprevalence of toxoplasmosis in females than males is consistent with various reports published globally
(Ramzan et al., 2009; Othman and Al-Azuheir, 2014). However, on the other hand few workers
(Ntafis et al., 2007; Caballero-Ortega et al., 2008) reported no association between gender and seropositivity.
