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. 2020 Spring;21(2):126–129.

Seroprevalence and associated risk factors of Toxoplasma gondii in sheep in Erzurum province, Eastern Anatolia region, Turkey

M S Aktaş 1,*, Ö Aydın 2
PMCID: PMC7430368  PMID: 32849892

Abstract

Background:

Toxoplasmosis causes economic losses due to abortion, neonatal death and reproductive diseases in infected sheep. Erzurum is one of the most important cities in Turkey where sheep farming is done. Aims: The aim of this study was to evaluate seroprevalence of Toxoplasma gondii and related risk factors in sheep brought to the slaughterhouse in Erzurum province of Eastern Anatolia region, Turkey.

Methods:

Nine-hundred and sixty sheep brought to slaughterhouse from Erzurum center and districts were used in this study. The data on age, breed, abortion history of sheep and whether or not they had contact with cats were recorded. The presence of T. gondii antibodies was determined by enzyme-linked immunosorbent assay (ELISA) kit in blood samples taken from sheep just before slaughter.

Results:

According to the study results, 44 (4.58%) of 960 sheep were found to be seropositive. Seroprevalence was found to be highest in the ≥2<3 age group with 5.29% (P>0.05), and it was more common in Akkaraman breed compared to Morkaraman breed (P<0.01). It was determined that 43 (97.73%) of the 44 seropositive sheep had contact with cats (P<0.01) and 12 of them (27.27%) had abort history.

Conclusion:

The study results identify the presence of T. gondii in the sheep from Erzurum province of Eastern Anatolia region, Turkey.

Key Words: Risk factors, Seroprevalence, Sheep, Toxoplasma gondii

Introduction

Toxoplasma gondii is an apicomplexan, obligate intracellular protozoan parasite and a pathogen capable of infecting almost all mammals and birds (Dubey, 2002 ▶). Toxoplasma gondii in sheep was first diagnosed in 1954 (Jones and Dubey, 2012) ▶, and it is well known that sheep are an important intermediate host of T. gondii (Tzanidakis et al., 2012 ▶). Toxoplasma gondii causes economic losses due to abortion, neonatal death and reproductive diseases in infected sheep (Thaller et al., 2011 ▶; Hammond-Aryee et al., 2015 ▶) and is also of zoonotic importance as it can be transmitted to humans through contaminated meat and milk (De Santana Rocha et al., 2015 ▶; Amairia et al., 2016 ▶).

Various risk factors associated with T. gondii have been reported in sheep including age, presence of cat in the farm, the size of the farm, climate conditions and geographical location (Abu Samra et al., 2007 ▶; Andrade et al., 2013 ▶). In addition, some sheep breeds are reported to be more susceptible to T. gondii infection than others (Dubey and Welcome, 1998 ▶; Williams et al., 2005 ▶). In adult sheep, infection may be subclinical, but often the only symptom is abortion (Hassing et al., 2003 ▶).

In seroprevalence studies conducted on sheep in different areas/cities in Turkey for T. gondii, seropositivity was determined between 13% and 99.19% (Akoz et al., 2009 ▶; Cicek et al., 2011 ▶). There are not any studies on the seroprevalence of T. gondii in sheep in Erzurum province, Eastern Anatolia region, Turkey.

The total number of small ruminant in the province of Erzurum is 717.843 and its share in the Eastern Anatolian region is approximately 19.3% (Kopuzlu et al., 2016 ▶). Therefore, the region has an important place in sheep farming. The aim of this study was to determine the seroprevalence of T. gondii and to evaluate risk factors such as age, breed, contact with cats and presence of abortion in sheep brought to the slaughterhouse in Erzurum province in the Eastern Anatolia region of Turkey.

Materials and Methods

Study area and animal

This study was conducted between May-November 2015 in Erzurum (39° 57′ 23″ N 41° 10′ 12″ E) which is located in the Eastern Anatolia region of Turkey. In this study, 960 sheep were used from city center of Erzurum and from its districts brought to the slaughterhouse located in Erzurum. Sheep breed, age, from which district, contact with cats and abort history were recorded according to the information received from the animal owner (Ethical Committee Decision Number: 2014/6).

Blood samples were taken from the vena jugularis of the sheep into sterile tubes without anticoagulant tubes (BD Vacutainer System, Plymouth, UK) just before the slaughtering and were centrifuged at 1.000 g for 15 min at 4°C to separate the serums. The obtained serums were kept at -80°C until analyses. All samples were analyzed at the same time.

Serological investigations

A commercial enzyme-linked immunosorbent assay (ELISA) kit was used for the detection of T. gondii in sheep serum samples (CHEKIT TOXOTEST, IDEXX Laboratory, USA). The kit was used in accordance with the manufacturer’s instructions.

Statistical analysis

Chi-square independence test was used to determine statistical significance between age groups and breeds in T. gondii seropositive sheep. Chi-square test was used to determine statistical significance between those who have aborted or not, and those who have contact with cats or not. Significant level was determined as P<0.05. SPSS 20.0 package program was used in the analysis.

Results

In this study, 44 (4.58%) of 960 sheep were positive for antibodies against T. gondii. Overall seroprevalence of T. gondii antibodies in sheep in Erzurum and districts were given in Table 1.

Table 1.

Overall seroprevalence of T. gondii antibodies in sheep in Erzurum and districts

District No. tested No. positive Seroprevalence (%)
Aşkale 10 4 40
Aziziye (central district) 52 0 0
Çat 58 8 13.80
Horasan 82 0 0
Karayazı 38 2 5.30
Palandöken (central district) 145 8 5.51
Pasinler 170 5 2.94
Tekman 60 8 13.33
Tortum 30 0 0
Şenkaya 155 5 3.22
Yakutiye (central district) 160 4 2.50
Total 960 44 4.58
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Seroprevalence of T. gondii antibodies in sheep according to age groups were given in Table 2. When the distribution of the age factor was evaluated statistically, it was determined that there was no significant difference between the age groups (P>0.05).

Table 2.

Seroprevalence of T. gondii antibodies in sheep according to age groups

Age groups (year) No. tested No. positive Seroprevalence (%)
≥1<2 32 0 0
≥2<3 472 25 5.29
≥3<4 413 19 4.60
≥4<6 43 0 0
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Seroprevalence of T. gondii antibodies in sheep according to breed groups were given in Table 3. It was determined that the difference between breed was significant statistically (P<0.01).

Table 3.

Seroprevalence of T. gondii antibodies in sheep according to breed groups

Sheep breed No. tested No. positive Seroprevalence (%)
Akkaraman 105 12 11.43a
Morkaraman 855 32 3.74b
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Different letters (a, b) indicate significant differences at P<0.01

It was determined that 27.27% of the sheep were positive against T. gondii antibodies have abortion history (P<0.01).

In the study, 97.73% of the seropositive sheep had contact with cats (P<0.01), while 2.27% of those without contact were identified.

Discussion

Different seroprevalence studies have been performed in sheep at different provinces in Turkey from 1976 to 2014. The lowest seropositivity rate was found in Konya province with 13%, and the highest rate was found in Afyon province with 99.19% (Akoz et al., 2009 ▶; Cicek et al., 2011 ▶). Although there is no study performed in Erzurum on T. gondii seroprevalence in sheep, Altintas (1975) ▶ reported that in 1975 sheep brought from Erzurum to Ankara for slaughter had a seropositivity rate of 31%. In this study, 4.58% seropositivity was determined in sheep brought for slaughter from Erzurum and its districts, and this rate is the lowest in seroprevalence studies that have been made on sheep until now in Turkey. It is known that arid, sub arid, high altitude and cold climate areas are not suitable for the survival of T. gondii oocysts, whereas humid, rainy, hot and low altitude areas are more suitable for them (Gebremedhin et al., 2014 ▶; Ahmed et al., 2016 ▶). Summers are short and arid, winters are long, snowy and very cold in Erzurum. Furthermore, Erzurum, with an altitude of 1860 meters above sea level is the highest province in Turkey. The reason for the T. gondii seroprevalence being lower in Erzurum compared to other regions in Turkey is probably in connection with its climate and geographical structure.

When T. gondii seropositivity was evaluated according to age, different results and different interpretations depending on these results emerged. It is indicated that the seroprevalence increases with age in sheep (Dubey, 2009 ▶; Ahmad, 2015 ▶; Hammond-Aryee et al., 2015 ▶). Puije et al. (2000) ▶ suggest that the reason of the increase in seroprevalence with age is that older animals are exposed to risk factors for a longer period of time. Lashari and Tasavar (2010) ▶, reported that seropositivity was most commonly seen at 16-28 months old and lowest at 68-80 months. It is indicated that this situation may be due to the poor resistance of T. gondii to animals aged 16-28 months (Jabar and Jori, 2013 ▶). In the presented study, although there was no statistical difference between ages, the highest positive rate was found in the ≥2<3 age group with 5.29% and then in the ≥3<4 age group with 4.60%. Similar to this study, Hammond-Aryee et al. (2015) ▶ determined that highest seropositivity was between 28-40 months.

Infected sheep may not always show clinical signs of toxoplasmosis, but often the most important symptom is abortion (Dubey, 2009 ▶). It is indicated that the T. gondii seropositivity in sheep with abortion is reported to 35.18% in Kayseri (Inci et al., 1999 ▶), 46.8% in Elazığ (Aktas et al., 2000 ▶), 97.4% in Kars (Mor and Arslan, 2007 ▶), 96% in Silopi during the studies performed in Turkey (Leblebicier and Yildiz, 2014 ▶). In this study, it has been determined that 12 of 44 sheep (27.27%) had an abortion history according to the anamnesis data from animal owners.

The cats are both final and intermediate hosts of the T. gondii and they have a vital role in the spread of oocysts and in transmission of the infection to other species. Therefore, the cat presence is an important factor that increases risk of possible infection in sheep (Ahmad et al., 2015 ▶). Studies on T. gondii sero-prevalence and risk factors in sheep have also shown that cats have intense contact with sheep (Leblebicier and Yildiz, 2014 ▶; Ahmad et al., 2015 ▶). In this study, 43 (97.73%) of 44 seropositive sheep had contact with cats, supporting previous studies.

Some researchers reported that some sheep breeds were more susceptible to T. gondii than other breeds (Williams et al., 2005 ▶). However, Sevgili et al. (2005) ▶, in a study conducted in Akkaraman, Ivesi and Morkaraman sheep in the Sanliurfa region, determined that there was no statistical difference between the breeds in terms of seropositivity. In this study, Akkaraman and Morkaraman sheep were used, and it was found that Akkaraman sheep were more sensitive than Morkaraman sheep and this difference was statistically significant. Ahmad et al. (2015) ▶ found that salt range sheep were more sensitive than another breed.

In conclusion, the study results identify the presence of T. gondii in the sheep from Erzurum province of Eastern Anatolia region, Turkey. The data obtained from this first study to determine the seroprevalence of T. gondii in the sheep in Erzurum province shows that cats are an important factor in the spread of the infection. For this reason, contamination of the special feed and water of the sheep with cat feces should be prevented. Although the determined seropositivity rate in this study is low compared to other studies in different regions of Turkey, it should be considered because the disease threatens both animal and human health. In addition, it is necessary to carry out extensive studies to determine prevalence, control and prevent of T. gondii in sheep in Erzurum province.

Acknowledgment

The financial source of this study was supported by Ataturk University Scientific Research Projects Unit (project No.: 2015/60).

Conflict of interest

The authors declare that they have no conflict of interest.

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