Open Access Open Access  Restricted Access Subscription Access
Cover Image

Serological and molecular studies of ovine and human toxoplasmosis with a trial of treatment of infected ewe

H.F. Khater, N. O. Khalifa, A.M. A. Barakat


The aims of the present study were to diagnose toxoplasmosisin pregnant ewes and women serologically and molecularly, treat naturallyinfected ewes, and diagnose congenital toxoplasmosis.  Blood samples were taken from 30 and 60pregnant ewes and women, respectively, and used for diagnosis of toxoplasmosisthrough Latex agglutination test (LAT). Seropositive samples were confirmed byPCR for detection of acute infection. Ten infected pregnant ewes wereclassified into two groups. The first group was treated with sulfadimidine33.3%, 200 mg (0.6 ml) / kg.b.wt, and the other group was treated with normalsaline. At titers ≥ 1:64, serological diagnosis indicated that 16 (53.33%) ewesand 29 (48.3%) women were seropositive and the seroprevalence increased in olderewe and younger women.  Positive LATsamples were used for amplification of DNA and showed bands at 193 bp,analogues to that of the RH strain in 12 (40%) and 15 (25%) blood samples ofewes and women, respectively. All treated ewes with sulfadimidine 33.3%delivered healthy lambs with normal gestation period, whereas untreated ewesdelivered 4 abortuses and 3 stillbirths. The tissue cysts were demonstratedmicroscopically in stained smears from tissues of dead fetuses.  Local strain of T. gondii was isolatedthrough intra peritoneal injection in mice from tissues of abortuses andstillbirths and maintained in the lab. The DNA of both RH (a virulent strain) andthe local strains expressed diagnostic amplified DNA bands at 193 bp,indicating a zoonotic importance of T. gondii and the role of sheep a assource of human infection.


Abdi, J., Shojaee, S., Mirzaee, A., et al., 2008. Seroprevalance of toxoplasmosis in pregnant women in Ilam proviance, Iran.Iranian J. Parasitol., 3(2), 34-37.

Abu Samra, N., McCrindle, C.M.E, Penzhorn, B.L., Cenci-Goga, B., 2007. Seroprevalence of toxolasmosis in sheep in South Africa. J. S. Afr. Vet. Assoc., 78, 116–120.

Abu-Dalbouh, M.A., Ababneh, M.M., Giadinis, N.D., Lafi, Sh.Q., 2012. Ovine and caprine toxoplasmosis (Toxoplasma gondii) in aborted animals in Jordanian goat and sheep flocks. Trop. Anim. Health. Prod., 44 (1), 49-54.

Acici, M., Babur, C., Kilic, S., Hokelek, M., Kurt, M. 2008. Prevalece of antibodies to Toxoplasma gondii infection in humans and domestic animals in Samsun province, Turkey. Trop. Anim. Health Prod., 40, 311–315.

Aly, S., Elsherbiny, M., Sand, M., Tohamy, A., 2004. Serodiagnosis of acute Toxoplasma gondii infection using ELIS and Immunoblotting.Egypt J. Biochim.Molec. Biol., 22, 476-488.

Andrade, M.M.C., Carneiro, M., Medeiros, A.D., Neto, V.A., Vitor, R.W.A., 2013. Seroprevalence and risk factors associated with ovine toxoplasmosis in Northeast Brazil. Parasite., 20, 20.

Asthana, S.P., Macpherson, C.N., Weiss, S.H., Stephens, R., Denny, T.N., Sharma, R.N., Dubey, J. P., 2006. Seroprevalence of Toxoplasma gondii in pregnant women and cats in Grenada, West Indies. J. Parasitol., 92, 644–645.

Azab, M.E., El-Shenawy, S.F., El-Hady, H.M., Ahmad, M.M., 1993. Comparative study of three tests (indirect haemagglutination direct agglutination, and indirect immuno-fluorescence) for detection of antibodies to Toxoplasma gondii in pregnant women. J. Egypt. Soc. Parasitol., 23,471–476.

Bastien, P., 2002. Molecular diagnosis of toxoplasmosis. Trans. R. Soc. Trop. Med. Hyg., 96 (suppl 1), s205-15.

Batz, M.B., Hoffmann, S., Morris, Jr., JG., 2012. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J. Food Prot., 75, 1278–1291.

Behbehani, K., Al-Karmi , T., 1980. Epidemiology of toxoplasmosis in Kuwait. I. Detection of antibodies to Toxoplasma gondii and percentage distribution among the inhabitants. Trans. R. Soc. Trop. Med. Hyg., 74, 209–212.

Burg, J. L., Grover, C.M., Pouletty, P., Boothroyd, J.C., 1989. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J. Clin. Microbiol., 27, 1787-1792.

Buxton, D., Rodger, S.M., 2007. Toxoplasmosis and neosporosis, in: Diseases of Sheep, 4th edn. Blackwell Publishing, London., pp. 112-119.

Buxton, D., Thmson, K.M., Maley. S., 1993. Treatment of ovine toxoplasmosis with a combination of sulphamezathine and pyrimethamine. Vet. Rec., 132, 409-411.

Buxton, D., Wright, S., Maley, S.W., Thomson, K.M., Brebner.J., et al., 1996. Decoquinate and the control of experimental ovine toxoplasmosis. Vet. Rec., 138, 434-436.

Buxton, D., Blewett, D.A., Trees, A.J., McColgan, C., Finlayson, J., 1988. Further studies in the use of monensin in the control of experimental ovine toxoplasmosis. J. Comp. Pathol., 98, 225-236.

Buxton, D., Maley, S.W., Wright, S.E., Rodger, S., Bartley, P., et al., 2007. Toxoplasma gondii and ovine toxoplasmosis: New aspects of an old story. Vet. Parasitol., 149, 25-28.

Cabannes, A., Lucchese, F., Hernandez, J., 1997. Enquete seroepide-miologique sur Toxoplasma gondii chez les ovins, bovines et felins dans le department de le Gironde. Bull. Soc. Fr. Parasitol., 15, 11- 22.

Centers for Disease Control and Prevention, CDC, 2011. CDC Estimates of Foodborne Illness in the United States>, insulted on January 25, 2011.

Dahbi, A., Bellete, B., Flori, P., Hssaine, A., Elhachimi, Y., et al., 2010.The effect of essential oils from Thymus broussonetii Boiss on transmission of Toxoplasma gondii cysts in mice.Parasitol.Res. 107 (1), 55-58.

Derouin, F., Sarfati, C., Beauvais, B., Iliou, M.C., Dehen, L., et al., 1989. Laboratory diagnosis of pulmonary toxoplasmosis in patients with acquired immunodeficiency syndrome. J. Clin. Microbiol., 27, 1661–1663.

Dubey, J., Frenkel, J., 1972. Cyst-induced toxoplasmosis in cats. J. Parasitol., 19, V.

Dubey, J., 2001. Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. J. Parasitol., 87, 215- 219.

Dubey, J., 2008. The history of Toxoplasma gondii -the first 100 years. J. Euk. Microbiol. 55, 467-475.

Dubey, J.P., 2009. Toxoplasmosis in sheep—The last 20 years. Vet. Parasitol., 163, 1–14.

Dubey, J.P., 2010. Toxoplasmosis of Animals and Humans, 2nd ed. CRC Press, Boca Raton, Florida, USA, pp. 1–313.

Dubey, J., Jones, J., 2008. Toxoplasma gondii infection in humans and animals in the United StatesInt.J. Parasitol., 38: 1257-1278.

Dubey, J.P., Grahamb, D.H., Dahl. E., Hilali, M., El-Ghaysh, A., Sreekumar, C., et al., 2003. Isolation and molecular characterization of Toxoplasma gondii from chickens and ducks from Egypt. Vet. Parasitol., 114, 89–95.

Dubey, J.P., 1996. Pathogenecity and infectivity of Toxoplasma gondii oocysts for rats. J. Parasitol., 82, 951-956.

Dubey, J.P., Beattie, C.P., 1988. Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, pp.1-220.

Dubey, J.P., Shen, S.K., Kwok, O.C., Frenkel, J.K., 1999. Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J. Parasitol., 85(4), 657-662.

Edwards, J.F., Dubey, J.P., 2013. Toxoplasma gondii abortion storm in sheep on a Texas farm and isolation of mouse virulent atypical genotype T. gondii from an aborted lamb from a chronically infected ewe. Vet. Parasitol., 192, 129– 136

El Ridi, A.M., Nada, S.M., Aly, A.S., Habeeb, S.M., Aboul-Fattah, M.M., 1990. Serological studies on toxoplasmosis in Zagazig slaughterhouse. J. Egypt. Soc. Parasitol., 20, 677–681.

El-Ghaysh, A., 1998. Seroprevalence of Toxoplasma gondii in Egyptian donkeys using ELISA. Vet. Parasitol., 80(1), 71-73.

El-Ghaysh, A.A., Mansour, M.M., 1994. Detection of antibodies to Toxoplasma gondii in an Egyptian sheep-herd using modern serological techniques. J. Egypt Assoc. Immunol., 1, 117–121.

El-Gozamy, B.R., Mohamed, S.A., Mansour, H.A., 2009. Toxoplasmosis among pregnant women in Qualyobia Governorate, Egypt.J. Egypt. Soc. Parasitol., 39(2), 389-401.

El-Tras, W.F., Tayel.A.A., El-Kady, N.N., 2011. Source diversity of Toxoplasma gondii infection during meal preparation. J. Food Saf., 32, 1-5.

Frenkel, J., Ruiz, A., Chinchilla, M., 1975. Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am. J. Trop. Med. Hyg., 24, 439-443.

Giadinis, N., Terpsidis, K., Diakou, A., Siarkou, V., Karatzias, H. et al., 2009. Treatment of sheep toxoplasmosis with sulfadimidine. In: Proceedings of the World Sheep Veterinary Congress, Stavanger, Norway.

Giadinis, N.D., Terpsidis, K., Diakou, A., Siarkou, V., Loukopoulos, P., et al., 2011. Massive toxoplasma abortions in a dairy sheep flock and therapeutic approach with different doses of sulfadimidine.Turk. J. Vet. Anim. Sci., 35(3), 207-211.

Guy, E.C., Joynson, D.H.M., 1995. Potential of the polymerase chain reaction in the diagnosis of active Toxoplasma infection by detection of parasite in blood. J. Infect. Dis., 172,319–322.

Haberkorn, A. 1996. Chemotherapy of human and animal coccidioses: state and perspectives. Parasitol. Res. 82, 193–199.

Habibi, G.R., Imani, A.R., Gholami, M.R., Hablolvarid, M.H., Behroozikhah, A.M., Lotfi, M., Kamalzade, M., Najjar, E., Esmaeil-Nia, K., Bozorgi, S., 2012. Detection and identification of Toxoplasma gondii type one infection in sheep aborted fetuses in Gazvin province of Iran. Iranian J. Parasitol., 7 (3), 64-72.

Harps, O., 1993. Untersuchungen u‥ ber die Seropra. valenz von Toxoplasma- Infektionen bei kleinen Wiederka‥ueren in Jordanien. D.V.M.Thesis. Hannover, Germany., pp. 1–137.

Hartley, W.J., Jebson, J.L., McFarlane, D., 1954. New Zealand type II abortion in ewes. Aust. Vet. J. 30, 216–218.

Hide, G., Morley, E.K., Hughes, J.M., Gerwash, O., Elmahaishi, M.S., et al., 2009. Evidence for high levels of vertical transmission in Toxoplasma gondii. Parasitol., 136, 1877–1885.

Hill, D., Dubey, J.P., 2002. Toxoplasma gondii: transmission, diagnosis and prevention. Clin.Microbiol. Infect., 8(10), 634-640.

Hussein, A.H., Ali, A.E., Saleh, M.H., Nagaty, I.M., Rezk, A.Y., 2001. Prevalence of toxoplasma infection in Qualyobia governorate, Egypt.J Egypt. Soc. Parasitol., 31(2), 355-63.

Hussein, A.H., Nagaty, I.M., Fouad, M.A., 2002. Evaluation of IgMELISA versus PCR in diagnosis of recent Toxoplasma gondii infection. J. Egypt. Soc. Parasitol., 32,639–646.

Ibrahim, H.M., Huang, P., Salem, T.A., Talaat, R.M., Nasr, M.I., et al., 2009. Short Report: Prevalence of Neospora caninum and Toxoplasma gondii Antibodies in Northern Egypt. Am. J. Trop. Med. Hyg., 80(2), 263–267.

Iqbal, J., Khalid, N., 2007. Detection of acute Toxoplasma gondii infection in early pregnancy by IgG avidity and PCR analysis. J. Med. Microbiol., 56, 1495–1499.

Johnson, M.A., McDonald, P.J., Neoh, H.S., 1979. Kinetics of the growth of Toxoplasma gondii (RH strain) in mice. Int. J. Parasitol., 9, 55-56.

Kamani, J., Mani, A.U., Egwu, G.O., 2010. Seroprevalence of Toxoplasma gondii infection in domestic sheep and goats in Borno state, Nigeria.Trop. Anim. Health Prod., 42 (4), 793-797.

Katzer, F., Brülisauer, F., Collantes-Fernández, E., Bartley, P.M., Burrells, A., Gunn, G., Maley, S.W., Cousens, C.,Innes, E.A., 2011. Increased Toxoplasma gondii positivity relative to age in 125 Scottish sheep flocks; evidence of frequent acquired infection. Vet. Res., 2011, 42(1), 121.

Khalifa, N.O., Mohamed, A.M., Aml- Hassen., 2005. Toxoplasmosis in animal and pregnant women in Kaliobia Governorate.Suez Canal Vet. Med. J., 8(2), 119-126.

Khalil, K.M., Elrayah, I.E., 2011. Seroprevalence of Toxoplasma gondii antibodies in farm animals (camels, cattle, and sheep) in Sudan. J. Med. Anim. Health., 3(3), 36-39.

Kijlstra, A., Jongert, E., 2008. Control of the risk of human toxoplasmosis transmitted by meat. Int. J. Parasitol., 38, 1359–1370.

Kul, O., Yildiz, K., Ocal, N., Freyre, A., Deniz, A., Siyami Karahan, S., Atmaca, H.T., Gokpinar, S., Dincel, G.C., Uzunaliog˘lu. T., Terzi, O.S., 2013. In-vivo efficacy of toltrazuril on experimentally induced Toxoplasma gondii tissue cysts in lambs: A novel strategy for prevention of human exposure to meat-borne toxoplasmosis. Res. Vet. Sci., 94, 269–276.

Lehmann, T., Marcet, P.L., Graham, D.H., Dahl, E.R., Dubey, J.P., 2006. Globalization and the population structure of Toxoplasma gondii. Proc. Nal. Academy Sci., 103, 11423-11428.

Lin, M., Chen, T., Kuo, T., Tseng, C., Tseng, C., 2000. Real time PCR for quantitative detection of Toxoplasma gondii. J. Clin. Microbiol., 38, 4121-5.

Mazumder, P., Chuang, H.Y., Wentz, M.W., Wiedbrauk , D.L ., 1988. Latex agglutination test for detection of antibodies to Toxoplasma gondii. J. Clin. Microbiol., 26, 2444–2446.

Menotti, J., Garin, Y., Thulliez, P., Sérugue, M., Stanislawiak, J., Ribaud, P., et al., 2010. Evaluation of a new 5'-nuclease real-time PCR assay targeting the Toxoplasma gondii AF146527 genomic repeat. Clinic. Microbiol. Infec., 16, 363-368.

Mitchell, S.M., Zajac, A.M., Davis, W.L., Lindsay, D.S., 2004. Efficacy of ponazuril in vitro and in preventing and treating Toxoplasma gondii infections in mice. J. Parasitol., 90, 639–642.

Moazeni Jula, F., Moazeni Jula, G., Nowzari, N., Kavari, H., Hashemzadeh Farhang, H., 2013. A Serological and Molecular study on Toxoplasma gondii infection in sheep and goat in Tabriz. Arch. Razi. Inst. 68 (1), 29-35.

Mobini, S., Heath, A.M., Pugh, D.G., 2002. Theriogenology of sheep and goats. In: Sheep and Goat Medicine, Saunders, Philadelphia., 183-184.

Mohammad, M., Ahmed, S., Hussain, A., 2012. Seroprevalence of Toxoplasma gondii in couples in Ramadi City using enzyme linked immunosorbent assay (ELISA). Int. J. Med. Med. Sci. 4(3): 55-59.

Molina-Boli´Var , J.A., Galisteo-Gonza´ Lez, F., 2005. Latex Immunoagglutination Assays. J. Macromol. Sci. Polymer Rev., 45, 59–98.

Mor, N., Arslan, M.O., 2007. Kars yo‥ resindeki koyunlarda Toxoplasma gondii nin seroprevalansi. Kafkas. Univ. Vet. Fak.Derg. 13: 165–170.

Nimri, L., Pelloux, H., Elkhatib, L., 2004. Detection of Toxoplasma gondii DNA and specific antibodies in high-risk pregnant women. Am. J. Trop. Med. Hyg., 71,831–835.

Oncel, T., Vural, G., 2006. Occurrence of Toxoplasma gondii antibodies in sheep in Istanbul. Turkey. Veterinarski.Arhiv., 76, 547–553.

Owen, M.R., Clarkson, M.J., Trees, A.J., 1998. Acute phase toxoplasma abortions in sheep. Vet. Rec. 142, 480–482.

Prelezov, P., Koinarski, V., Georgieva, D., 2008. Seroprevalence of Toxoplasma gondii infection among sheep and goats in the Stara Zagora region. Bulgarian J. Vet. Med., 11, 113–119.

Ramadan, M.Y., Abdel- Mageed, A.F., Khater, H.F., 2007. Seroprevalence and preliminary treatment of toxoplasmosis of pregnant goats in Kalubyia Governorate, Egypt. Acta Sci. Vet., 36 (3), 295- 301.

Remington, J.S., Mcleod, R., Desmonts, G., 1995. Toxoplasmosis. In: Remington JS, Klein JO (eds) Infectious Diseases of the Fetus and Newborn Infant. W. B. Saunders Co. Philadelphia., pp, 140–267.

Romand, S., Franck, J., Thulliez, P., Peyron, F., Dumon ,H., 2001. Prenatal diagnosis using polymerase chain reaction on amniotic fluid for congenital toxoplasmosis. Obstet. Gynecol. 97, 296-300.

Samad, M.A., Dey, B.C., Chowdhury, N.S., Akhtar, S., Khan, M.R., 1997. Seroepidemiological studies on Toxoplasma gondiii infection in man and animals in Bangladesh. Southeast Asian J. Trop. Med. Publ. Hlth., 28, 393-343.

Sawadogo, P., Hafid, J., Bellete, B., Sung, R.T.M., Chakdi, M., Flori, P., Raberin, H., Hamouni, I.B., Chait, A., Dalal, A., 2005. Seroprevalence of T. gondii in sheep from Marrakech, Morocco. Vet. Parasitol., 130, 89–92.

Schares, G., Vrhovec, M., Pantchev, N., Herrmann, D., Conraths, F., 2008. Occurrence of Toxoplasma gondii and Hammondia hammondi oocysts in the faeces of cats from Germany and other European countries. Vet. Parasitol., 152, 34-45.

Shaapan, R.M., Abo-ElMaaty, A.M., Abd El-Razik, K.A., Abd El-Hafez, S.M., 2012. PCR and serological assays for detection of Toxoplasma gondii infection in sport horses in Cairo, Egypt. Asian J. Anim. Vet. Adv., 70, 158-165.

Shaapan, R.M., El-Nawawi, F.A., Tawfik, M.A.A., 2008. Sensitivity and specificity of various serological tests for the detection of Toxoplasma gondii infection in naturally infected sheep. Vet. Parasitol., 153, 359–362.

Shaapan, R.M., Fathia Khalil, A.M., 2008. Evaluation of different Toxoplasma gondii isolates as antigens used in the modified agglutination test for the detection of toxoplasmosis in camels and donkeys. Am. Eurasian J. Agric. Environ. Sci., 3 (6), 837-841.

Smokovitis, A., 1990. The udder. In: Physiology, 2nd ed., Kyriakidis co, Th essaloniki., 506-549.

Suzuki, Y., 2002. Host resistance in the brain against Toxoplasma gondii.J. Infec. Dis., 185, 58-65.

Tavassoli, M., Esmaeilnejad, B., Tabatabaei, M., et al., 2009. A survey on infection of animals with Toxoplasma gondii using PCR and genetic differences using RFLP in Urmia, Iran. Pazhoohesh va Sazandegi 58, 61-66.

Tavassoli, M., Ghorbanzadehghan, M., Esmaeilnejad, B., 2013. Detection of Toxoplasma gondii in sheep and goats blood samples by PCR-RFLP in Urmia. Vet. Res., Forum 4 (1), 43 – 47.

Tenter, A., Heckeroth, A., Weiss, L., 2001. Toxoplasma gondii: from animals to humans. Internl. J. Parasitol., 31, 217-220.

Torrey, E.F., Bartko, J.J., Yolken, R.H., 2012. Toxoplasma gondii and other risk factors for schizophrenia: an update. Schizophr. Bull., 38 (3), 642–647.

Van de Ven, E., Melchers, J., Galama, J., Camps, W., Meuwissen, J., 1991. Identification of Toxoplasma gondii infections by B1 gene amplification. J. Clin. Microbiol., 29, 2120–2124.

Vesco, G., Buffolano, W., La Chiusa, S., Mancuso, G., Caracappa, S., Chianca, A., Villari, S., Curro`, V,, Liga F, Petersenl E. 2007. Toxoplasma gondii infections in sheep in Sicily, southern Italy. Vet. Parasitol., 146, 3–8.

Vimercati, A., Greco, P., D’apolito, A., Angelici, M.C., Possenti, A., Carbonara, S., et al., 2000. Risk assessment of vertical transmission of Toxoplasma infections. Acta Biomed Ateneo Parmense., 71 (Suppl 1), 537–540.

Vitale, M., Currò, V., Giglia, M.L., Vitale, F., Goździk, K., Caracappa, S., 2008. A nested PCR for Toxoplasma gondii detection from different animal samples. Wiadomooeci Parazytologiczne, 54 suplement 19.

Wahab, T., Edvinsson, B., Palm, D., Lindh, J., 2010. Comparison of the AF146527 and B1 repeated elements, two realtime PCR targets used for detection of Toxoplasma gondii. J. Clinic. Microbiol., 48, 591-602

Wainwright, K., Miller, M., Barr, B., Gardner, I., Melli, A., Essert, T., Packham, A., Truong, T., Lagunas-Solar, M., Conrad, P., 2007. Chemical inactivation of Toxoplasma gondii oocysts in Water. J. Parasitol., 93, 925–931.

Webster, J.P., Kaushik, M., Bristow, G.C., McConkey, G.A., 2013. Toxoplasma gondii infection, from predation to schizophrenia: can animal behaviour help us understand human behaviour? J. Exp. Biol., 216 (1), 99–112.

Williams, R.H., Morley, E.K., Hughes, J.M., Duncanson, P., Terry, R.S., Smith, J.E., Hide, G., 2005. High levels of congenital transmission of Toxoplasma gondii in longitudinal and cross-sectional studies on sheep farms provides evidence of vertical transmission in ovine hosts. Parasitol., 130, 301–307.

Zaki, M., 1995.Seroprevalence of Toxoplasma gondii in domestic animals in Pakistan. J. Pakistan Med. Assoc., 45, 4-5.

Full Text: PDF


  • There are currently no refbacks.