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Seroprevalence of Toxoplasma gondii infection and associated risk factors among pregnant women in Sebha region, Libya
Corresponding Author(s) : Nosseur M. El-sayed
International Journal of Allied Medical Sciences and Clinical Research,
Vol. 4 No. 3 (2016): 2016 Volume 4- Issue -3
Abstract
M. El-sayed
ABSTRACT
Toxoplasmosis is one of the most common worldwide parasitic diseases caused by an obligate intracellular
protozoan parasite Toxoplasma gondii. It is commonly transmitted to humans by accidental ingestion of oocysts
voided in cat feces or tissue cyst in meat. Congenital transmission may occur when an uninfected mother
acquires primary infection during pregnancy. The acquired infection is usually asymptomatic, while congenital
one may lead to abortion, stillbirth or severe abnormalities in the newborn. A tota l of 190 pregnant women were
interviewed with questionnaire about known risk factors (age, residence and occupational status, raw vegetables
and fruits intake, source of drinking of water, milk intake, frequency of meat intake, consumption of raw,
undercooked meat or processed meat, frequency of eating in restaurant and fast food outlet, co ntact with cat and
soil, history of pregnancy, abortion and blood transfusion). The collected sera were tested for detection of
immunoglobulins (IgG&IgM) against T. gondii using Enzyme Linked Fluorescent Assay (ELFA) with the
VIDAS Toxo-competition kit (BioMérieux, France).A total of 70 (36.84%) out of 190 pregnant women sera
were seropositive for Toxoplasma gondii specific IgG antibodies, while all examined women were seronegative
for IgM. Seroprevalence of T. gondii IgG antibodies in respect to previously mentioned risk factors were
statistically non-significant (P>0.05).
Keywords
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Weiss, L.M.and Dubey,J.P. "Toxoplasmosis: A history of clinical observations". International Journal for Parasitology. 39(8), 2009, 895–901.
[2]. Afonso,E.; Thulliez, P. and Gilot-Fromont, E. Transmission of Toxoplasma gondii in an urban population of domestic cats (Feliscatus). Int. J. Parasitol. 36, 2006, 1373–1382
[3]. Robert-GangneuxF. and Dardé, M. Epidemiology of and Diagnostic Strategies for Toxoplasmosis. Clin. Microbiol. Rev. 25(2), 2012, 264-296
[4]. Montoya, J.G and Liesenfeld, O. Toxoplasmosis. 363, 2004, 11-22, 1965–1976
[5]. Jones, J.L. and Dubey, J.P. "Food borne toxoplasmosis". Clinical Infectious Diseases: an Official Publication of the Infectious Diseases Society of America 55(6), 2012, 845–51.
[6]. Jones, J.L.; Kruszon-Moran, D.;Wilson, M.; McQuillan,G.;Navin,T. and McAuley, J.B. "Toxoplasma gondii infection in the United States: seroprevalence and risk factors". American Journal of Epidemiology 154 (4), 2001, 357–65.
[7]. Herwaldt, B.L. Laboratory-acquired parasitic infections from accidental exposures. Clin. Microbiol. 14, 2001, 659–688.
[8]. Desmonts, G. and Couvreur J. Congenital toxoplasmosis. A prospective study of 378 pregnancies. N. Engl. J. Med. 290, 1974, 1110–1116.
[9]. Remington,J.S; McLeod, R.;Thulliez, P. and Desmonts, G. Toxoplasmosis, In Remington JS, Klein J (ed), Infectious diseases of the fetus and newborn infant, 5th ed. WB Saunders, Philadelphia, PA. 2001, 205-346, 205–346
[10]. Hill, D. and Dubey,J.P. "Toxoplasma gondii: transmission, diagnosis and prevention". Clinical Microbiology and Infection: the Official Publication of the European Society of Clinical Microbiology and Infectious Diseases. 8(10), 2002, 634–40.
[11]. Montoya,J.G "Laboratory diagnosis of Toxoplasma gondii infection and toxoplasmosis". The Journal ofInfectious Diseases. 185(1), 2002, 73–82
[12]. Hung, C.C; Fan, C.K.; Su K.E; Sung, F.C; Chiou, H .Y. and Gil, V. Serological screening and toxoplasmosis exposure factors among pregnant women in the Democratic Republic of Sao Tome and Principe. Trans. R. Soc. Trop.Med .Hyg. 101(2), 2007, 134-139.
[13]. El Said,M. M. A.; Azbedah,A.G.; EL-Alem, D.E. and Alkout, A. The prevalence of Toxoplasma gondii infection in psychiatric patients in Tripoli, Libya. Journal of American Science 10(5), 2014, 135-140.
[14]. Legnain, M.; Singh, R. and Prawecka, M. Prevalence of Toxoplasma antibodies and pregnancy wastage among women in Benghazi with pertinent review of literature. Garyounis Medical Journal. 6(1), 1992, 69-77.
[15]. Swalem, A. and Feturi, A. Prevalence of antibodies to Toxoplasma gondii in pregnant women and in different age groups in Benghazi. Garyounis Medical Journal 17(1-2), 1994, 14-20.
[16]. Legnain, M. M. and Prawecka, M. Prevalence of Toxoplasma Antibodies and Pregnancy Wastage among Women in Benghazi with Pertinent Review of Literature. GaryounisMedical Journal l6 (1), 1983, 69-77.
[17]. Kassem, H. H. and Morsy,T. A. The Prevalence of Anti-Toxoplasma Antibodies among Pregnant Women in Benghazi, (S.P.L.A.J.) Libya'. J. Egypt. Soc.Parasitol. 1, 1991, 69-74.
[18]. Mousa, D.A.; Mohammad, M.A. and Toboli, A.B. Toxoplasma gondii infection in pregnant women with previous adverse pregnancy outcome.Medical Journal of Islamic Academy of Science 19(2), 2011, 95-102.
[19]. Alkateb, A.; Flamer,O; Bellasher, A; Shakshoky,G; Albellazy,M. and Abudher,A. Role of the meat in transmission of toxoplasmosis. Infectious and endemic disease.Abstracts of the Technical programmed.Scientific conference (IEDSC) Tripoli, Libya 83, 2007.
Nosseur S et al / Int. J. of Allied Med. Sci. and Clin. Research Vol-4(3) 2016 [383-391]
390
[20]. Magrhi,S.; Abudher, A. ; Guma,N; Hagrasi,H. ;Mohammed, S.; Musbah,M.;Ali M. and Abeed,S. Toxoplasmosis and Pregnancy outcome', second national Biotechnology Conference proceeding Book Albeda, 2003, 435-442.
[21]. Gashout, A.; Lazrag, T; Gashut,H. and Swedan,T Qualitative assessment of risk for spontaneous abortion associated with Toxoplasma and Rubella: immunity appraisal . The Libyan Journal of Infectious Diseases 2, 2008, 52-65.
[22]. Khader, M.A. and El Nageh, M. M. (1987): Serological Survey for Toxoplasmosis in Tripoli, S.P.L.A.J. (Libya)'. Trans R Soc Trop Med.Hyg. 81(5), 2008, 761-763.
[23]. Abu Setta, A. M. and Yamani, R. H. 'Prevalence of Toxoplasmosis in Non-Pregnant Women in Tripoli, Libya', .The Egyptian Journal of Hospital Medicine l(31), 2008, 198-202. [24]. Shaddel, M; MirzaiiDizgah, I.and Sharif, F. The prevalence of toxoplasmosis in Imam Reza Hospital blood bank samples, Tehran, Iran. TransfusApher Sci.TransfusApher Sci. 14, 2014, 156-6.
[25]. Ghazi, H.O.; Telmesani, A.M.; Mahomed, M.F. TORCH agents in pregnant Saudi women. Med .Princ.Pract. 11(4), 2002, 180-2.
[26]. Alvarado-Esquivel, C.; Pacheco-Vega1, S .J; Hernández-Tinoco, J. ;Sánchez-Anguiano, L. ;Berumen-Segovia, L.O.; Rodríguez-Acevedo, F .J. I. ;Beristain-García, I. ;Rábago-Sánchez, E. , Liesenfeld O. ;Campillo-Ruiz,F.andGüereca-García, O. A. Seroprevalence of Toxoplasma gondii infectionand associated risk factors in Huicholes in Mexico . Parasites &Vectors 7, 2014, 301-308.
[27]. Zemene,E.;Yewhalaw,D.;Abera,S.; Belay, T.; Samuel,A.and Zeynudin,A., Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women in Jimma town, Southwestern Ethiopia . BMC Infectious Diseases. 12, 2012, 337-342
[28]. Yobi, D.;Piarroux, R.;Ollivier,C. L.; Franck, J. ;Situakibanza, H.;Muhindo, H. ;Mitashi, P.; Inocêncio, R.A. ; Sprundel, M.V. ; Boelaert,M. ; VanGeertruyden, J.; and Lutumba,P. Toxoplasmosis among pregnant women: High seroprevalence and risk factors in Kinshasa, Democratic Republic of Congo . Asian Pac. J .Trop. Biomed. 4(1), 2014, 69-74. [29]. Da Silva, M G ;Câmara, J.T, Vinaud,M.C and De Castro A.M. Epidemiological factors associated with seropositivity for toxoplasmosis in pregnant women from Gurupi, State of Tocantins, Brazil. Rev. Soc. Bras. Med. Trop. 47(4), 2014, 469-475. [30]. El Deeb, H.K. ;Salah-Eldin, H. ;Khodeer, S.andAllah, A.A. Prevalence of Toxoplasma gondii infection in antenatal population in Menoufia governorate.Egypt.ActaTrop.124(3), 2012, 185-91
[31]. Mohamed, K.; Ahmed, A .A. and Elrayah,I .E. Prevalence and risk factors for Toxoplasma gondii infection in humans from Khartoum State,Sudan.Int. J. Public Health Epidemiol. 23, 2013, 60-66.
[32]. Al-Nakib, W. Seroepedemiology of viral and Toxoplasma infections during pregnancy among Arab women of childbearing age in Kuwait .Int.J.Epid. 12(2), 1983, 220-3.
[33]. Nimri, L.; Pelloux, H. and Elkhatib, H. Detection of T. gondii DNA and specific antibodies in high-risk pregnant women. Am. J .Trop. Med. Hyg. 71(6), 2004, 831-5.
[34]. Abbas, S. ; Basalamah, A. ; Serebour, F. and Afonso, M. The prevalence of Toxoplasma gondii antibodies in Saudi women and the outcome of congenital infection among newborns in Saudi Arabia. Saudi med .J. 7(4) 1986, 346-54 .
[35]. El Mansouri, B. ;Rhajaoui, M. and Sebti, F. Seroprevalence of toxoplasmosis in pregnant women in Rabat, Morocco. Bull .Soc.Pathol.Exot. 100(4), 2007, 289-90.
[36]. Mahdi, N. and Sharief, M. Risk factors for acquiring toxoplasmosis in pregnancy. Bahrain Med .Soc. J. 14(4), 2002, 148-51.
[37]. Mwambe, B. ; E Mshana, S. ;Kidenya, B .R. ; Massinde, A. N.; Mazigo Humphrey, D. ; Michael D; Majinge, C. and Groß, U. Sero-prevalence and factors associated with Toxoplasma gondii infection among pregnant women attending antenatal care in Mwanza,Tanzania . Parasites &Vectors 6, 2013, 222-227. [38]. Gencer, M.; Cevizci, S. ; Saçar, S. ; Vural, A. ; Cak?rGüngör, A.N. ; Uysal, A. ;Hac?velio?lu, S.Ö. ; Celik M. ;Duru, Eand Co?ar, E. Evaluation of anti-Toxoplasma gondii antibody distribution and risk factors among pregnant women admitted to obstetrics polyclinic of CanakkaleOnsekiz Mart University Hospital].TurkiyeParazitolDerg. 38(2), 2014, 76-80.
Nosseur S et al / Int. J. of Allied Med. Sci. and Clin. Research Vol-4(3) 2016 [383-391]
391
[39]. Salibay, C.; Dungca, J .and Claveria, F. Serological survey of Toxoplasma gondiiinfection among Urban (Manila) and Suburban (Dasmariñas, Cavite) Residents, Philippines. J. Proto. Res. 18, 2008, 26-33.
[40]. Han, K. ; Shin, D. ; Lee, T. and Lee, Y Seroprevalence of Toxoplasma gondii Infection and Risk Factors Associated with Seropositivity of Pregnant Women in Korea. J.Parasi. 94(4), 2008, 963–65.
[41]. Pappas,G. ; Roussos,N. and Falagas, M.E. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. J. Parasitol. 39, 2009, 1385–1394.
[42]. Afonso.E.;Thulliez, P. and Gilot-Fromont,E. Local meteorological conditions, dynamics of seroconversion to Toxoplasma gondii in cats (Feliscatus) and oocyst burden in a rural environment.Epidemiol. Infect. 138, 2010, 1105–1113.
[43]. Dubey, J .P. Toxoplasmosis of animals and humans, CRC Press, Boca Raton, FL, 2, 2010.
[44]. Al-Qurashi, A.R.; Gander, A. M.;Obeid, O. E.;Al-Mulhim, A. and Makki,S.M. Seroepidemiological study of Toxoplasma gondii Infection in the Human Population in the Eastern Region. Saudi Med. J. 22(1), 2001, 13.
[45]. Buratbine, A.; Silages Chahed, M. K. and Ben Ismail, R. Seroepidemiology profile of toxoplasmosis in northern Tunisia .Parasite. 8(1), 2001, 61-62
[46]. Hao, Y Difference of Toxoplasma gondii infection status between urban and rural childbearing age women visiting to hospitals in southwest region of Shandong Province. ZhongguoXue Xi Chong Bing Fang ZhiZaZhi, 25(1), 2013, 113–114.
[47]. Cook, A.J.; Gilbert, R.E.; Buffolano, W. ; Zufferey, J. ;Petersen, E.andJenum, P.A. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. British Med. J. 321, 2000, 142-147
[48]. Avelino, M.M.; Campos-Júnior, D.; Parada, J.B. and Castro, A.M. Risk factors for Toxoplasma gondii infection in women of childbearing age. The Braz. J. Infect. Dis. 8, 2004, 164-174
[49]. Bowie,W.R.; King, A.S.;Werker, D.H.; Isaac-Renton, J.L.; Bell, A.;Eng,S.B. and Marion,S.A. Outbreak of toxoplasmosis associated with municipal drinking water. Lancet, 350, 1997, 173–177.
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References
[2]. Afonso,E.; Thulliez, P. and Gilot-Fromont, E. Transmission of Toxoplasma gondii in an urban population of domestic cats (Feliscatus). Int. J. Parasitol. 36, 2006, 1373–1382
[3]. Robert-GangneuxF. and Dardé, M. Epidemiology of and Diagnostic Strategies for Toxoplasmosis. Clin. Microbiol. Rev. 25(2), 2012, 264-296
[4]. Montoya, J.G and Liesenfeld, O. Toxoplasmosis. 363, 2004, 11-22, 1965–1976
[5]. Jones, J.L. and Dubey, J.P. "Food borne toxoplasmosis". Clinical Infectious Diseases: an Official Publication of the Infectious Diseases Society of America 55(6), 2012, 845–51.
[6]. Jones, J.L.; Kruszon-Moran, D.;Wilson, M.; McQuillan,G.;Navin,T. and McAuley, J.B. "Toxoplasma gondii infection in the United States: seroprevalence and risk factors". American Journal of Epidemiology 154 (4), 2001, 357–65.
[7]. Herwaldt, B.L. Laboratory-acquired parasitic infections from accidental exposures. Clin. Microbiol. 14, 2001, 659–688.
[8]. Desmonts, G. and Couvreur J. Congenital toxoplasmosis. A prospective study of 378 pregnancies. N. Engl. J. Med. 290, 1974, 1110–1116.
[9]. Remington,J.S; McLeod, R.;Thulliez, P. and Desmonts, G. Toxoplasmosis, In Remington JS, Klein J (ed), Infectious diseases of the fetus and newborn infant, 5th ed. WB Saunders, Philadelphia, PA. 2001, 205-346, 205–346
[10]. Hill, D. and Dubey,J.P. "Toxoplasma gondii: transmission, diagnosis and prevention". Clinical Microbiology and Infection: the Official Publication of the European Society of Clinical Microbiology and Infectious Diseases. 8(10), 2002, 634–40.
[11]. Montoya,J.G "Laboratory diagnosis of Toxoplasma gondii infection and toxoplasmosis". The Journal ofInfectious Diseases. 185(1), 2002, 73–82
[12]. Hung, C.C; Fan, C.K.; Su K.E; Sung, F.C; Chiou, H .Y. and Gil, V. Serological screening and toxoplasmosis exposure factors among pregnant women in the Democratic Republic of Sao Tome and Principe. Trans. R. Soc. Trop.Med .Hyg. 101(2), 2007, 134-139.
[13]. El Said,M. M. A.; Azbedah,A.G.; EL-Alem, D.E. and Alkout, A. The prevalence of Toxoplasma gondii infection in psychiatric patients in Tripoli, Libya. Journal of American Science 10(5), 2014, 135-140.
[14]. Legnain, M.; Singh, R. and Prawecka, M. Prevalence of Toxoplasma antibodies and pregnancy wastage among women in Benghazi with pertinent review of literature. Garyounis Medical Journal. 6(1), 1992, 69-77.
[15]. Swalem, A. and Feturi, A. Prevalence of antibodies to Toxoplasma gondii in pregnant women and in different age groups in Benghazi. Garyounis Medical Journal 17(1-2), 1994, 14-20.
[16]. Legnain, M. M. and Prawecka, M. Prevalence of Toxoplasma Antibodies and Pregnancy Wastage among Women in Benghazi with Pertinent Review of Literature. GaryounisMedical Journal l6 (1), 1983, 69-77.
[17]. Kassem, H. H. and Morsy,T. A. The Prevalence of Anti-Toxoplasma Antibodies among Pregnant Women in Benghazi, (S.P.L.A.J.) Libya'. J. Egypt. Soc.Parasitol. 1, 1991, 69-74.
[18]. Mousa, D.A.; Mohammad, M.A. and Toboli, A.B. Toxoplasma gondii infection in pregnant women with previous adverse pregnancy outcome.Medical Journal of Islamic Academy of Science 19(2), 2011, 95-102.
[19]. Alkateb, A.; Flamer,O; Bellasher, A; Shakshoky,G; Albellazy,M. and Abudher,A. Role of the meat in transmission of toxoplasmosis. Infectious and endemic disease.Abstracts of the Technical programmed.Scientific conference (IEDSC) Tripoli, Libya 83, 2007.
Nosseur S et al / Int. J. of Allied Med. Sci. and Clin. Research Vol-4(3) 2016 [383-391]
390
[20]. Magrhi,S.; Abudher, A. ; Guma,N; Hagrasi,H. ;Mohammed, S.; Musbah,M.;Ali M. and Abeed,S. Toxoplasmosis and Pregnancy outcome', second national Biotechnology Conference proceeding Book Albeda, 2003, 435-442.
[21]. Gashout, A.; Lazrag, T; Gashut,H. and Swedan,T Qualitative assessment of risk for spontaneous abortion associated with Toxoplasma and Rubella: immunity appraisal . The Libyan Journal of Infectious Diseases 2, 2008, 52-65.
[22]. Khader, M.A. and El Nageh, M. M. (1987): Serological Survey for Toxoplasmosis in Tripoli, S.P.L.A.J. (Libya)'. Trans R Soc Trop Med.Hyg. 81(5), 2008, 761-763.
[23]. Abu Setta, A. M. and Yamani, R. H. 'Prevalence of Toxoplasmosis in Non-Pregnant Women in Tripoli, Libya', .The Egyptian Journal of Hospital Medicine l(31), 2008, 198-202. [24]. Shaddel, M; MirzaiiDizgah, I.and Sharif, F. The prevalence of toxoplasmosis in Imam Reza Hospital blood bank samples, Tehran, Iran. TransfusApher Sci.TransfusApher Sci. 14, 2014, 156-6.
[25]. Ghazi, H.O.; Telmesani, A.M.; Mahomed, M.F. TORCH agents in pregnant Saudi women. Med .Princ.Pract. 11(4), 2002, 180-2.
[26]. Alvarado-Esquivel, C.; Pacheco-Vega1, S .J; Hernández-Tinoco, J. ;Sánchez-Anguiano, L. ;Berumen-Segovia, L.O.; Rodríguez-Acevedo, F .J. I. ;Beristain-García, I. ;Rábago-Sánchez, E. , Liesenfeld O. ;Campillo-Ruiz,F.andGüereca-García, O. A. Seroprevalence of Toxoplasma gondii infectionand associated risk factors in Huicholes in Mexico . Parasites &Vectors 7, 2014, 301-308.
[27]. Zemene,E.;Yewhalaw,D.;Abera,S.; Belay, T.; Samuel,A.and Zeynudin,A., Seroprevalence of Toxoplasma gondii and associated risk factors among pregnant women in Jimma town, Southwestern Ethiopia . BMC Infectious Diseases. 12, 2012, 337-342
[28]. Yobi, D.;Piarroux, R.;Ollivier,C. L.; Franck, J. ;Situakibanza, H.;Muhindo, H. ;Mitashi, P.; Inocêncio, R.A. ; Sprundel, M.V. ; Boelaert,M. ; VanGeertruyden, J.; and Lutumba,P. Toxoplasmosis among pregnant women: High seroprevalence and risk factors in Kinshasa, Democratic Republic of Congo . Asian Pac. J .Trop. Biomed. 4(1), 2014, 69-74. [29]. Da Silva, M G ;Câmara, J.T, Vinaud,M.C and De Castro A.M. Epidemiological factors associated with seropositivity for toxoplasmosis in pregnant women from Gurupi, State of Tocantins, Brazil. Rev. Soc. Bras. Med. Trop. 47(4), 2014, 469-475. [30]. El Deeb, H.K. ;Salah-Eldin, H. ;Khodeer, S.andAllah, A.A. Prevalence of Toxoplasma gondii infection in antenatal population in Menoufia governorate.Egypt.ActaTrop.124(3), 2012, 185-91
[31]. Mohamed, K.; Ahmed, A .A. and Elrayah,I .E. Prevalence and risk factors for Toxoplasma gondii infection in humans from Khartoum State,Sudan.Int. J. Public Health Epidemiol. 23, 2013, 60-66.
[32]. Al-Nakib, W. Seroepedemiology of viral and Toxoplasma infections during pregnancy among Arab women of childbearing age in Kuwait .Int.J.Epid. 12(2), 1983, 220-3.
[33]. Nimri, L.; Pelloux, H. and Elkhatib, H. Detection of T. gondii DNA and specific antibodies in high-risk pregnant women. Am. J .Trop. Med. Hyg. 71(6), 2004, 831-5.
[34]. Abbas, S. ; Basalamah, A. ; Serebour, F. and Afonso, M. The prevalence of Toxoplasma gondii antibodies in Saudi women and the outcome of congenital infection among newborns in Saudi Arabia. Saudi med .J. 7(4) 1986, 346-54 .
[35]. El Mansouri, B. ;Rhajaoui, M. and Sebti, F. Seroprevalence of toxoplasmosis in pregnant women in Rabat, Morocco. Bull .Soc.Pathol.Exot. 100(4), 2007, 289-90.
[36]. Mahdi, N. and Sharief, M. Risk factors for acquiring toxoplasmosis in pregnancy. Bahrain Med .Soc. J. 14(4), 2002, 148-51.
[37]. Mwambe, B. ; E Mshana, S. ;Kidenya, B .R. ; Massinde, A. N.; Mazigo Humphrey, D. ; Michael D; Majinge, C. and Groß, U. Sero-prevalence and factors associated with Toxoplasma gondii infection among pregnant women attending antenatal care in Mwanza,Tanzania . Parasites &Vectors 6, 2013, 222-227. [38]. Gencer, M.; Cevizci, S. ; Saçar, S. ; Vural, A. ; Cak?rGüngör, A.N. ; Uysal, A. ;Hac?velio?lu, S.Ö. ; Celik M. ;Duru, Eand Co?ar, E. Evaluation of anti-Toxoplasma gondii antibody distribution and risk factors among pregnant women admitted to obstetrics polyclinic of CanakkaleOnsekiz Mart University Hospital].TurkiyeParazitolDerg. 38(2), 2014, 76-80.
Nosseur S et al / Int. J. of Allied Med. Sci. and Clin. Research Vol-4(3) 2016 [383-391]
391
[39]. Salibay, C.; Dungca, J .and Claveria, F. Serological survey of Toxoplasma gondiiinfection among Urban (Manila) and Suburban (Dasmariñas, Cavite) Residents, Philippines. J. Proto. Res. 18, 2008, 26-33.
[40]. Han, K. ; Shin, D. ; Lee, T. and Lee, Y Seroprevalence of Toxoplasma gondii Infection and Risk Factors Associated with Seropositivity of Pregnant Women in Korea. J.Parasi. 94(4), 2008, 963–65.
[41]. Pappas,G. ; Roussos,N. and Falagas, M.E. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int. J. Parasitol. 39, 2009, 1385–1394.
[42]. Afonso.E.;Thulliez, P. and Gilot-Fromont,E. Local meteorological conditions, dynamics of seroconversion to Toxoplasma gondii in cats (Feliscatus) and oocyst burden in a rural environment.Epidemiol. Infect. 138, 2010, 1105–1113.
[43]. Dubey, J .P. Toxoplasmosis of animals and humans, CRC Press, Boca Raton, FL, 2, 2010.
[44]. Al-Qurashi, A.R.; Gander, A. M.;Obeid, O. E.;Al-Mulhim, A. and Makki,S.M. Seroepidemiological study of Toxoplasma gondii Infection in the Human Population in the Eastern Region. Saudi Med. J. 22(1), 2001, 13.
[45]. Buratbine, A.; Silages Chahed, M. K. and Ben Ismail, R. Seroepidemiology profile of toxoplasmosis in northern Tunisia .Parasite. 8(1), 2001, 61-62
[46]. Hao, Y Difference of Toxoplasma gondii infection status between urban and rural childbearing age women visiting to hospitals in southwest region of Shandong Province. ZhongguoXue Xi Chong Bing Fang ZhiZaZhi, 25(1), 2013, 113–114.
[47]. Cook, A.J.; Gilbert, R.E.; Buffolano, W. ; Zufferey, J. ;Petersen, E.andJenum, P.A. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. British Med. J. 321, 2000, 142-147
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