This study was carried out in order to determine the occurrence of Toxoplasma gondii antibodies in sheep in five districts of Istanbul, Turkey. A total of 181 sera taken from sheep were examined for antibodies to Toxoplasma gondii using an enzyme-linked immunosorbent assay (ELISA). Of the 181 samples tested 56 (31%) were determined as seropositive. The prevalence of Toxoplasma antibodies was significantly higher in adult sheep (P0.05). These results indicate that ovine toxoplasmosis is widespread in Istanbul. To our knowledge, this is the first report on the status of T. gondii infection in sheep in Istanbul.Istraživanje je provedeno sa svrhom da se ustanovi nalaz protutijela za protoozon Toxoplasma gondii u ovaca s pet područja Istanbula u Turskoj. Ukupno je bilo pretražen 181 uzorak seruma imunoenzimnim testom. Specifična protutijela bila su dokazana u 56 (31%). Prevalencija protutijela bila je značajno veća u odraslih ovaca (P0,05). Rezultati potvrđuju veću proširenost ovčje toksoplazmoze i ujedno predstavljaju i prvo izvješće o stanju bolesti u Istanbulu

Gulay Vural

Taraneh Oncel

English

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547VETERINARSKI ARHIV 76 (6), 547-553, 2006* Contact address:Dr. Taraneh Oncel, Department of Parasitology, Veterinary Control and Research Institute, Pendik, 34890, Istanbul, Turkey, Phone: +90 216 3901 280; Fax: +90 216 3547 692; E-mail: taranehoncel@hotmail.comISSN 0372-5480Printed in CroatiaOccurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyTaraneh Oncel*, and Gulay VuralDepartment of Parasitology, Veterinary Control and Research Institute, Pendik, Istanbul, TurkeyONCEL, T., G. VURAL: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, Turkey. Vet. arhiv 76, 547-553, 2006. ABSTRACTThis study was carried out in order to determine the occurrence of Toxoplasma gondii antibodies in sheep in five districts of Istanbul, Turkey. A total of 181 sera taken from sheep were examined for antibodies to Toxoplasma gondii using an enzyme-linked immunosorbent assay (ELISA). Of the 181 samples tested 56 (31%) were determined as seropositive. The prevalence of Toxoplasma antibodies was significantly higher in adult sheep (P<0.001). No significant difference between male and female sheep groups was observed (P>0.05). These results indicate that ovine toxoplasmosis is widespread in Istanbul. To our knowledge, this is the first report on the status of T. gondii infection in sheep in Istanbul.Key words: enzyme-linked immunosorbent assay, sheep, Toxoplasma gondii, TurkeyIntroductionToxoplasmosis is a widespread zoonosis caused by the coccidian protozoan Toxoplasma gondii. It is an important cause of abortion, stillbirth and neonatal mortality in sheep (DUBEY and BEATTIE, 1988). The definitive hosts of the parasite are domestic cats and other felines, the sexual cycle occurring only in these species (FRENKEL et al., 1970). Human toxoplasmosis can be acquired both through ingestion of sporulated oocysts and via ingestion of bradyzoites in the tissues of numerous food animals. The infection is also transmitted transplacentally (DUBEY, 1994; ESTEBAN-REDONDO et al., 1995). Transmission of T. gondii tachyzoites in unpasteurised sheep or goat milk and blood transfusions can occur, but are probably not important epidemiologically (SCHIRLEY, 1995). The diagnosis of Toxoplasma infection is conventionally made by the direct demonstration or isolation of the parasite from biopsy or autopsy material, but such 548 Vet. arhiv 76 (6), 547-553, 2006techniques are unsuitable for use in large-scale surveys. Therefore, recourse has been made to immunoserological tests for specific host antibody, and a variety of tests have been described (ANDERSON and REMINGTON, 1975). Numerous reports from various countries exist on the prevalence of toxoplasmosis. It is estimated that 35-40% of the world’s adult population have been infected with T. gondii (SMITH, 1991). The prevalence rates in sheep have been varied among countries, as have the diagnostic methods used (HASHEMI-FESHARKI, 1996; PITA GONDIM et al., 1999; TENTER et al., 2000; HOVE et al., 2005). In Turkey, these rates were reported as being between 7.1% and 88.7% on regional basis. (WEILLAND and DALCHOW, 1970; ALTINTAS, 1996; BABUR et al., 2001)The prevalence of T. gondii in sheep in Istanbul has been unknown, thereby making it impossible to assess their potential significance to public health. The aim of the present study was to investigate the occurrence of antibodies to T. gondii among sheep in Istanbul, Turkey.Materials and methods A total of 181 serum samples were collected from sheep in Istanbul between February and November 2001. Istanbul is located at sea level, in north-west Turkey. Its western part T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyFig. 1. Map of Istanbul showing sampling districts549Vet. arhiv 76 (6), 547-553, 2006T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, Turkeyis in Europe and its eastern part is in Asia. Istanbul has a mild climate. The average annual humidity, temperature and precipitation are 74.9%, 14.6 ºC and 700.4 mm, respectively. Sheep were sampled by a simple random sampling method in five districts of Istanbul (Fig. 1). The sera were separated from blood samples by centrifugation and stored at -20 ºC until analysis. Information collected on sheep was age, sex and source of sheep. The age range was from 6 months to 8 years. Sheep IgG antibodies to T. gondii were tested by using an enzyme-linked immunosorbent assay (ELISA). The method was a modification of an ELISA previously described for human IgG antibodies to T. gondii (MONDESIRE et al., 1981). Positive and negative control sera were included on each plate. Anti-Sheep IgG horseradish peroxidase conjugate (Sigma Chemical Co., St. Louis, USA) was used. Reading was carried out at 492 nm using Titertek Multiskan Spectrophotometer. Results were analyzed statistically using the Chi-square test for significance in the present study. The analytical software package (Statistix Version 1.0., 1996) was used for the analysis.ResultsIn total, 56 (31%) samples by ELISA were found to be seropositive out of 181 blood samples in this study. Antibodies to T. gondii were found in all 5 districts sampled. Sheep sampled in Gaziosmanpasa had the highest prevalence (64.52%) of toxoplasmosis, while the lowest prevalence was found among sheep from Kartal (10%), as shown in Table 1. The seropositivity of toxoplasmosis in sheep from Tuzla, Silivri and Sile was 60%, 23.86% and 19.05%, respectively. Seroprevalence of T. gondii was significantly different according to the percentage of seropositive sheep present in each district (P<0.05). Table 1. T. gondii infected sheep according to district in Istanbul, TurkeyDistricts No of serum samples No of positives Seropositive rate* %Gaziosmanpsa 31 20 64.52aTuzla 10 6 60aSilivri 88 21 23.86bSile 42 8 19.05bKartal 10 1 10bTotal 181 56 31*Values having different superscripts were significantly different (P<0.05). 550 Vet. arhiv 76 (6), 547-553, 2006T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyThe association of age with the presence of infection is shown in Table 2. In Istanbul, seroprevalence was the highest in the ≥1-year-old age group. There was a significant difference between these two groups (P<0.001). Table 2. Age distribution of sheep with T. gondii infectionAge groups No of examined No of positives Seropositive rate %0.6-1 yr 64 8  12.5≥1-yr 117 48  41There was a significant difference between these two groups (P<0.001). Thirty-eight (31.40%) of 121 female sheep and 18 (30%) of 60 male sheep tested were seropositive for toxoplasmosis (Table 3). There was no significant difference between these two groups (P>0.05). Table 3. Sex distribution of sheep with T. gondii infectionSex No of examined No of positives Seropositive rate %Female 121 38 31.40Male 60 18 30There was no significant difference between these two groups (P>0.05). DiscussionToxoplasmosis is a zoonotic disease caused by T. gondii and has been known in many countries since 1908 (DUBEY and BEATTIE, 1988). SMITH (1991) reported that the prevalence of toxoplasmosis varies among countries, depending on traditions, customs and the life styles of the inhabitants. T. gondii infection in sheep is distributed worldwide, with prevalence rates ranging from 0% to 100% in different countries (DUBEY and BEATTIE, 1988; TENTER et al., 2000). It is therefore not possible to compare prevalence data of studies which used different serological tests with variable sensitivity and specificity. The prevalence of 31% for toxoplasmosis found in this study is lower than reported for sheep in Canada (57.6%) and Ghana (33.2%) but is higher than reported in Greece (23%) and Morocco (27.6%), where enzyme-linked immunosorbent assay was used (WALTNER-TOEWS et al., 1991; STEFANAKES et al., 1995; PUIJE et al., 2000; SAWADOGO et al., 2005). The 31% seropositivity rate detected in 181 sheep in Istanbul is lower than those reported previously in the other regions of Turkey (BABUR et al., 2001; TUTUNCU et al., 2003; ONCEL et al., 2005). This difference was concluded to be due to the fact that the studies were carried out in different geographical regions. However, our results demonstrate that T. gondii is widely distributed in the environment. 551Vet. arhiv 76 (6), 547-553, 2006T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyFor many authors (O’DONOGHUE et al., 1987; PUIJE et al., 2000), age is an important factor. Older sheep have a higher prevalence of toxoplasmosis than younger sheep. We found the highest prevalence in animals over one year of age. ALEXANDER and STINSON (1988) reported that female animals are more susceptible than males to infections with protozoan parasites. In the present study, no significant difference was observed between male and female groups (P>0.001).The high seroprevalence of T. gondii antibodies in sheep may be associated with the presence of cats in almost every farm sampled, and the probability that a young cat may shed oocysts on a farm will always be present. (WEILAND and DALCHOW, 1970; DUBEY, 1994). Infected cats excrete toxoplasma oocysts which, after sporulation, become infectious to man and animals, remaining infectious for a long time (GHORBANI et al., 1983). Higher prevalence rates of toxoplasmosis in warm, moist areas compared to those which are cold and dry is attributed to the longer viability of T. gondii oocysts in moist or humid environments (FAYER, 1981; PUIJE et al., 2000). Istanbul is a warm and moist area, which helps T. gondii oocysts to maintain their viability. In conclusion, the results of this study confirm the presence of toxoplasma antibodies in sheep in Istanbul. Toxoplasma infection among animals is of great importance, because some of the infected animals play a distinct role as a source of human infection. Finally, we emphasize that further studies are needed to clarify the impact of toxoplasmosis on the animal industry and losses due to clinical toxoplasmosis in livestock in Turkey. AcknowledgementsWe are grateful to Dr. Salih Yurtalan for critical comments on the statistical analysis.ReferencesALTINTAS, K. (1996): Toxoplasma gondii infections of animals in Turkey. Acta. Parasitol. Turcica 20, 479-487.ALEXANDER, J., W. H. STINSON (1988): Sex hormones and the course of parasitic infection. Parasitol. Today 4, 189-193.ANDERSON, S. E., J. S. REMINGTON (1975): The diagnosis of toxoplasmosis. Southern Med. J. 68, 1433-1443.BABUR, C., B. ESEN, G. BIYIKOGLU (2001): Seroprevalence of Toxoplasmosis gondii in Yozgat, Turkey. Tr. J. Vet. Anim. Sci. 25, 283-285.DUBEY, J. P. (1994): Toxoplasmosis. J. Am. Vet. Med. Assoc. 205, 1593-1597.DUBEY, J. P., C. P. BEATTIE (1988): Toxoplasmosis of animals and man. CRC Press, Boca Raton, Florida. pp. 61-80.552 Vet. arhiv 76 (6), 547-553, 2006T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyESTEBAN-REDONDO, I., S. W. MALEY, K. THOMSON, S. NICOLL, S. WRIGHT, D. BUXTON, E. A. INNES (1995): Detection of T. gondii in tissues of sheep and cattle following oral infection. Vet. Parasitol. 86, 155-171.FAYER, R. (1981): Toxoplasmosis update and public health implications. Can. Vet. 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KILIÇ (2005): Detection of Toxoplasmosis gondii in sheep in Yalova by Sabin Feldman Dye Test and Latex Agglutination Test. Acta. Parasitol. Turcica 29, 10-12.PITA GONDIM, L. F., H. V. BARBOSA, C. H. A. RIBEIRO FILHO, H. SAEKI (1999): Serological survey of antibodies to Toxoplasma gondii in goats, sheep, cattle and water buffaloes in Bahia State, Brazil. Vet. Parasitol. 82, 273-276.PUIJE, W. N. A., K. M. BOSOMPEM, E. A. CANACOO, J. M. WASTLING, B. D. AKANMORI (2000): The prevalence of anti-Toxoplasma gondii antibodies in Ghanian sheep and goats. Acta Tropica 76, 21-26.SAWADOGO, P., J. HAFID, B. BELLETE, R. T. SUNG, M. CHAKDI, P. FLORI, H. RABERIN, I. B. HAMOUNI, A. CHAIT, A. DALAL (2005): Seroprevalence of T. gondii in sheep from Marrakech, Morocco. Vet. Parasitol. 130, 89-92.SCHIRLEY, M. W. (1995): Vaccines against animal coccidiosis. Commission of the European Co-operation in Scientific and Technical Research (COST), Belgium, pp. 35-43.SMITH, J. L. (1991): Food borne toxoplasmosis. J. Food. Safety 12, 17-57.STEFANAKES, A., A. BIZAKE, E. KRAMBOVITES (1995): Serological survey of toxoplasmosis in sheep and goats on Crete. Bull. Hell. Vet. Med. Soc. 46, 243-249. TENTER, A. M., A. R. HECKEROTH, L. M. WEISS (2000): Toxoplasma gondii: from animals to humans. Int. J. Parasitol. 30, 1217-1258.TUTUNCU, M., E. AYAZ, M. YAMAN, H. A. AKKAN (2003): The seroprevalance of Toxoplasma gondii in sheep, goats and cattle detected by indirect heamagglutination (IHA) test in the region of Van, Turkey. Indian Vet. J. 80, 401-403.553Vet. arhiv 76 (6), 547-553, 2006T. Oncel and G. Vural: Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul, TurkeyWALTNER-TOEWS, D., R. MONDESIRE, P. MENZIES (1991): The seroprevalence of Toxoplasma gondii in Ontario sheep flocks. Can. Vet. J. 32, 734-737.WEILLAND, G., W. DALCHOW (1970): Toxoplasma Infektionen bei Haustieren in der Turkey (Serologische Untersuchungen im Sabin-Feldman-Test). Berl. Münich. Tierärztl. Wschr. 83, 65-68.ONCEL, T., G. VURAL: Nalaz protutijela za protozoon Toxoplasma gondii u ovaca u Istanbulu u Turskoj. Vet. arhiv 76, 547-553, 2006.SAŽETAKIstraživanje je provedeno sa svrhom da se ustanovi nalaz protutijela za protoozon Toxoplasma gondii u ovaca s pet područja Istanbula u Turskoj. Ukupno je bilo pretražen 181 uzorak seruma imunoenzimnim testom. Specifična protutijela bila su dokazana u 56 (31%). Prevalencija protutijela bila je značajno veća u odraslih ovaca (P<0,001). Nije utvrđena značajna razlika između mužjaka i ženki (P>0,05). Rezultati potvrđuju veću proširenost ovčje toksoplazmoze i ujedno predstavljaju i prvo izvješće o stanju bolesti u Istanbulu. Ključne riječi: imunoenzimni test, ovca, Toxoplasma gondii, TurskaReceived: 22 March 2005Accepted: 3 November 2006

Nalaz protutijela za protozoon Toxoplasma gondii u ovaca u Istanbulu u Turskoj.

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