Original Article
Seroprevalence of Toxoplasma gondii infection in ruminants in selected districts in Bangladesh

https://doi.org/10.1016/j.vprsr.2017.10.008Get rights and content

Abstract

To estimate the seroprevalence of toxoplasmosis and risk factors for seropositivity in sheep, goats and cattle in Dhaka, Mymensingh, Sirajganj and Chittagong districts in Bangladesh, 1104 sera samples (552 sheep, 300 goats and 252 cattle) were randomly selected and tested by an indirect enzyme linked immunosorbent assay (iELISA). The overall seroprevalence was 12.2% (135/1104), and was significantly (P = 0.008) higher in goats (16.0%) than cattle (8.3%). The odds of seropositivity was 2.09 times (95% confidence interval [CI]: 1.23–3.67) higher in goats than cattle. In sheep, herd type, district and pregnancy status were significant risk factors.

The odds of seropositivity was 2.1 (95% CI: 1.00–4.84), 7.29 (95% CI: 12.71–423.41) and 10.88 (95% CI: 5.42–23.41 times higher in sheep-only flocks, in Mymensingh district and in pregnant sheep than in mixed flocks, Chittagong district and non-pregnant sheep, respectively. In cattle, breeds and district were significant risk factors. The odds of seropositivity was 5.79 (95% CI: 1.13–24.62) and 4.29 (95% CI: 1.38–16.34) times higher in Holstein Friesian cross cattle and in Mymensingh district than in indigenous cattle and Chittagong district, respectively. This study indicates that exposure of sheep, goats and cattle to oocysts of T. gondii is widespread, suggesting that the consumption of raw and undercooked meat of these animals might be a source of human toxoplasmosis. Risk factor information can be used to design control programs to reduce exposure.

Introduction

Toxoplasma gondii is a multi-host obligate intracellular protozoan parasite, causing zoonotic infections throughout the world. It infects humans and a wide range of mammalian and avian species (Smith and Reduck, 2000). Toxoplasmosis causes congenital disease and abortion both in humans and livestock (Dubey and Beattie, 1988, Remington and Desmonts, 1990). Almost one third of the human population has been infected with this parasite worldwide (Montoya and Liesenfeld, 2004). Among food animals, sheep and goats are well-known sources of human infection (Dubey, 2010). In many countries, T. gondii is a major cause of reproductive disorders, miscarriages and abortions in the sheep industry, and therefore is responsible for substantial economic losses (Buxton et al., 2007, EFSA, 2007). Maternal toxoplasmosis during early pregnancy in humans can lead to death of the fetus or can cause chorioretinitis, hydrocephaly, microcephaly and jaundice in neonates (Joynson and Wreghitt, 2001, James, 2003).

Definitive hosts of this coccidian parasite are felids – both domestic and wild – whilst intermediate hosts are mammals and birds (Nematollahi and Moghddam, 2008, Dubey and Jones, 2008). The intermediate hosts are infected by ingesting food or water contaminated with oocysts, eating undercooked meat with tissue cysts or by transplacental infection with tachyzoites (Dubey and Jones, 2008, Dubey, 2010).

T. gondii infection is the major cause of abortion and perinatal mortality in sheep and goats worldwide (Buxton and Brebner, 1998). Abortion and neonatal mortality occur when sheep and goats suffer a primary infection during pregnancy. Sheep are considered important in the epidemiology of T. gondii infection worldwide, in general and Europe, in particular (Cook et al., 2000, Buxton et al., 2007). Ingestion of infected lamb serves as a direct source of infection for humans.

Currently there are several diagnostic procedures for determining T. gondii infection. The ELISA is well suited to laboratories in which large numbers of samples need to be analyzed (OIE, 2008). Numerous modifications of the ELISA have been reported to enhance specificity and to simplify the protocol of the conventional ELISA (Dubey and Beattie, 1988). The dye test is considered as the “gold standard” serological test at least in humans (OIE, 2008).

Cattle, goats and sheep are widely used as food animals in Bangladesh. Infection of herbivores occurs mostly via ingestion of T. gondii oocysts excreted by cats. In Bangladesh most cats are stray; they can be found in association with farm animals, and contaminate the environment by shedding oocysts. One week after a first infection, cats can shed over 100 million oocysts in their faeces for a period of 7–14 days depending on the infection dose, the infection stage and the immune status of the cat. Sporulated oocysts can remain infectious in the environment for > 1 year and contaminate pastures, feed and also drinking water (Dubey and Beattie, 1988, Innes et al., 2009). The reported seroprevalence of toxoplasmosis in cats varied from 33.33–36.36% (Samad et al., 1997, Hossain, 2016), whereas the seroprevalence of human toxoplasmosis varied from 10.66–38.5% (Samad et al., 1993, Samad et al., 1997, Ashrafunnessa et al., 1998, Margia, 2015, Hossain, 2016).

There have been a few studies reporting seroprevalence of T. gondii in sheep, goats and cattle in parts of Bangladesh. The range of reported seroprevalence of toxoplasmosis varied from 12–27% in cattle, 12–61% in goats and 18–69% in sheep (Samad et al., 1993, Shahiduzzaman et al., 2011, Rahman et al., 2014). However, sample sizes in these studies were small and the areas included were confined to only Mymensingh and Rajshahi districts. Moreover, the risk factors for toxoplasmosis in sheep, goats and cattle in Bangladesh have not been reported. Hence the objectives of this study were to estimate the seroprevalence of Toxoplasma gondii infection in sheep, goats and cattle and to investigate risk factors for seropositivity.

Section snippets

Study area and sampling design

The animal management system in Bangladesh is small scale dairy with traditional subsistence management systems. The small-scale dairy system mainly practices zero grazing (“cut-and-carry system”) with occasional tethering systems, mainly for goats. Occasionally when there are no crops in the field, different species of animals with different owners graze together in villages. Sheep are usually reared with zero input and mainly live on roadside grasses where they graze freely. Marginal and

Seroprevalence of toxoplasmosis in different species

The overall seroprevalence in domestic ruminants tested was 12.2% (95% confidence interval [CI]: 10.4–14.3). Species-specific seroprevalence is shown in Table 1. The seroprevalence of toxoplasmosis was significantly (P = 0.008) higher in goats than cattle. The odds of seropositivity was 2.09 times (95% CI: 1.23–3.67) higher in goats than cattle.

Seroprevalene of toxoplasmosis in sheep

Serology testing results for sheep are presented in Table 2. In bivariable analysis, sex, age, pregnancy status and herd composition were significantly

Discussion

We examined the seroprevalence of T. gondii infection in sheep, goats and cattle in Dhaka, Mymensingh, Chittagong and Sirajganj districts of Bangladesh. The overall seroprevalence we observed was 12.2%. The seroprevalence of toxoplasmosis has been reported to vary widely ranging from 3.3% in Mexico to 90.9% in The Netherlands (Dubey, 2010),

The seroprevalence of toxoplasmosis was found to be 16% in goats, 12% in sheep and 8% in cattle. These estimates are extremely low compared to previous

Conclusion

The considerable seroprevalence of toxoplasmosis in sheep, goats and cattle observed suggests that oocysts and reservoirs are widely dispersed in the environment and thus represent a risk to public health in Bangladesh. These food animals may serve as a potential source of infection for humans if their meat and milk are consumed raw or undercooked. Routine monitoring of T. gondii infection in these animals may be helpful in control of this zoonosis both in animals and humans in Bangladesh.

Conflict of interest statement

We declare no conflicts of interest.

Acknowledgement

The authors gratefully acknowledge the Ministry of Science and Technology, BS 53;2013-2014 Government of Bangladesh for funding this work (to Md Hasanuzzaman Talukder).

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