Taibah University

Journal of Taibah University Medical Sciences (2016) 11(3), 255e259

Journal of Taibah University Medical Sciences

www.sciencedirect.com

Original Article

Seroprevalence of Toxoplasma gondii among pregnant women in

Almadinah Almunawwarah KSA

Naglaa F.A. Imam, MDa,*, Esra’a A.A. Azzam, M. Sc. b and Ahmed A. Attia, MD c

aDepartment of Medical Parasitology, Faculty of Medicine, Cairo University, Cairo, EgyptbMedical Laboratories Technology Department, Taibah University, Almadinah Almunawwarah, KSAcGynecology and Obstetrics Department, Faculty of Medicine, Cairo University, Egypt

Received 27 January 2016; revised 11 April 2016; accepted 12 April 2016; Available online 7 May 2016

صخلملا

فشكلانإف٬ةيقلخلاتاهوشتلاولمحلاىلعتافعاضمللارظن:ثحبلافادهأفشكللةساردلاهذهفدهت.لمحلاءانثأةيمهأرثكأوهةيلوألاتاسوقملاءادنعخيراتنهيدليتاللالماوحلاءاسنلانيبةيدنوغلاةسوقملليلصملاراشتنالانع.لمتحمرطخنهيدلنوكيدقيتآللاوأتاسوقملاءادبيحوييضرم

نيبنهرامعأحوارتتلماوحءاسنلمدلصمةنيع١٥٠صحفمت:ثحبلاقرطجئاتنلاديكأتمت.عيرسلاةيدنوغلاةسوقملارابتخامادختسابكلذو،اماع٤٥و١٨

IgG.وIgMلازيلإةينقتةطساوباضيأ

ءوضيفايئاصحإتاسوقملاءادبةباصإللةيلصملاجئاتنلاليلحتمت:جئاتنلالجستملو،IgGلةيباجيإ)٪٣٫٢١(ةلاح٣٢تناكو.ةحاتملاةيئابولاتانايبلا.نيرابتخالاالكبIgMلةيباجيإةلاحيأ

ةباصإلاةيباجيإنيبةماهتاقالعكانهنأةساردلاترهظأ:تاجاتنتسالاتاهوشتبباصملفطةدالوصرفو٬ضاهجإلاخيراتو،مألارمعوضرملابنإف٬ةساردلاهذهيفةثيدحىودعىلعةلدأدوجومدعنممغرلاىلعو.ةيقلخاديدهتدعيلماوحلاءاسنلانيبةيدنوغلاةسوقملابةباصإلاتالدعمعافترا.لمحلاءانثأيلوألاضرعتلل

؛ةيدوعسلاةيبرعلاةكلمملا؛لمحلا؛ازيلإ؛ةرونملاةنيدملا:ةيحاتفملاتاملكلاعيرسلاتاسوقملارابتخا؛تاسوقملا

Abstract

Objectives: Given its detrimental obstetric and congential

sequelae, the detection of primary toxoplasmosis is most

* Corresponding address: Department of Medical Parasitology,

Faculty of Medicine, Cairo University, Cairo, Egypt.

E-mail: naglaa-fouad@hotmail.com (N.F.A. Imam)

Peer review under responsibility of Taibah University.

Production and hosting by Elsevier

1658-3612 � 2016 The Authors.Production and hosting by Elsevier Ltd on behalf of Taibah University. T

(http://creativecommons.org/licenses/by-nc-nd/4.0/). http://dx.doi.org/10.10

critical during pregnancy. This study aims to detect the

seroprevalence of Toxoplasma gondii (Toxoplasma gondii)

among pregnant women who either have histories sug-

gestive of toxoplasmosis or may be at risk.

Methods: Serum samples of 150 pregnant women aged 18

e45 years were tested by the rapid Toxoplasma test

(TOXO IgM/IgG test, InTec). The results were further

confirmed by the enzyme-linked immunosorbent assay

(ELISA) technique for IgM and IgG.

Results: Serological results of toxoplasmosis seropositivity

were statistically analyzed in light of the available epide-

miological data. Thirty-two cases (21.3%) were IgG posi-

tive, and none was IgM positive, as shown by both tests.

Conclusion: Significant relations were observed between

seropositivity, maternal age and history of abortion, and

probability of delivering a child with a congenital

anomaly. Despite the lack of evidence of recent infection

in this study, the high rates of T. gondii seropositivity

among pregnant women signaled a threat of primary

exposure during pregnancy.

Keywords: Almadinah Almunawwarah; ELISA; KSA;

Pregnancy; Toxoplasma; TOXO rapid test

� 2016 The Authors.Production and hosting by Elsevier Ltd on behalf of Taibah

University. This is an open access article under the CC BY-

NC-ND license (http://creativecommons.org/licenses/by-nc-

nd/4.0/).

his is an open access article under the CC BY-NC-ND license

16/j.jtumed.2016.04.004

http://creativecommons.org/licenses/by-nc-nd/4.0/http://creativecommons.org/licenses/by-nc-nd/4.0/mailto:naglaa-fouad@hotmail.comhttp://crossmark.crossref.org/dialog/?doi=10.1016/j.jtumed.2016.04.004&domain=pdfwww.sciencedirect.comhttp://creativecommons.org/licenses/by-nc-nd/4.0/http://dx.doi.org/10.1016/j.jtumed.2016.04.004http://dx.doi.org/10.1016/j.jtumed.2016.04.004http://dx.doi.org/10.1016/j.jtumed.2016.04.004

N.F.A. Imam et al.256

Introduction

Toxoplasma gondii is an obligatory intracellular proto-

zoan parasite that appears to have broad host specificityand the ability to penetrate various host cells.1 Mostindividuals exposed to Toxoplasma gondii are

asymptomatic or suffer a mild, non-specific and self-limiting illness. However, significant morbidity and mor-tality is observed when toxoplasmosis infects the fetus

(transplacentally) and immunocompromised persons, suchas patients with human immunodeficiency virus. Clinicalpresentation varies between these different patientgroups.1e3 Congenital transmission may occur when an

uninfected mother acquires primary infection duringpregnancy. Primary infection with T. gondii in pregnantwomen occurs all over the world with frequencies between

0.1% and 1%.1,4 Few studies have been conducted toexplore the seroprevalence of T. gondii among pregnantSaudi women, with varying results.5e8

Pregnant women with primary toxoplasmosis infectionare often asymptomatic or have only mild symptoms, andapproximately 70%e90% of infants born with congenitaltoxoplasmosis are asymptomatic at birth. Nevertheless,infection may cause spontaneous abortion, still birth, pre-maturity or serious fetal damage.2,9,10 This is becausetoxoplasmosis acquired in the first and second trimesters

of pregnancy generally shows a more severe degree ofillness in the newborn, although transplacental infection isleast likely during the first trimester.8e10 Newborns may

show signs such as epilepsy (or seizures at birth), anemia,jaundice, rash, hepatosplenomegaly, thrombocytopenia,encephalitis, pneumonitis, microcephaly, intracranial

calcification, hydrocephalus, diarrhea, hypothermia andnonspecific illness. Visual impairment, learning disabilitiesand mental retardation generally become apparent severalmonths to years later.1,10 Previously, premature infants in

KSA, with different clinical presentations, showed ananti-Toxoplasma IgM seropositivity of 23.1%.11

The mainstay for the diagnosis of toxoplasmosis is

serological testing for anti-Toxoplasma antibodies.Systematic serological screening for T. gondii IgG and IgMantibodies should be performed in all pregnant women as

early as possible in gestation (ideally in the first trimester)and in seronegative women each month.12 Diagnosisof acute maternal infection is mainly based on detection

of seroconversion, or fourfold rise in IgM antibodieslevel, which appear sooner after infection than IgGantibodies and disappear faster than IgG after recovery.1

Accurate, early diagnosis of congenital toxoplasmosis is

vital for proper treatment before fetal complicationsoccur.13e16 Other tests, such as the rapid dipstick test17

or IgG avidity tests, which are reported to be cost-

effective,18 and molecular techniques, such as polymerasechain reaction, are also helpful in differentiating acuterecent and old stages of toxoplasmosis during

pregnancy.18e20

Toxoplasma IgG/IgM dipstick rapid assays for therapid detection of IgG and IgM antibodies have becomepopular. This is because they are simple and easy, with

easily interpreted results and high sensitivity and speci-ficity.17e20

Materials and Methods

Serum specimens were collected from 150 pregnant Saudi

women in the first and second trimester, whose ages rangedfrom 19 to 44 years (mean age 29 � 4.2). Those below 20years of age were primiparous (with one previous birth and

one previous abortion). The rest were all multigravida andmultiparous. The study group attended the Maternity andChildren Hospital, Almadinah Almunawwarah, KSA, be-

tween January and June 2015. The study was approved bythe Research Ethical Board of the College of Applied Med-ical Sciences, Taibah University, as part of the procedure oftheir follow up at the hospital, including obtaining patients’

consent. They were chosen for either having history sugges-tive of congenital toxoplasmosis (abortion, child withcongenital anomaly), or risk factors such as cat contact,

along with a few patients with no such history. None of themwas previously tested for toxoplasmosis. Specimens wereeither refrigerated if not used on the day of collection, or

frozen if not used within 3 days of collection. Next, 0.1% ofsodium azide was added to the specimens as a preservativewith no effect on the assay results.19e21

All sera specimens were tested by the TOXO test (anti-Toxoplasma-IgM/IgG test, InTec Products Inc., China), thenconfirmed by ELISA technique for IgM and IgG detection(Behring ELISA processor III, BEP III) using the United

Diagnostic Industry kit (UDI, KSA). This ELISA processoruses photometry, which is a method determining the con-centration of finely suspended or dissolved substances in

samples. However, the absorbance cannot be measureddirectly. It is only possible to measure the intensities of theincident light and the transmitted light. The absorbance

value is calculated from these values.22

Rapid TOXO IgG/IgM test is a colloidal gold enhanced,rapid immunochromatographic assay for the qualitativedetection of IgG and IgM type antibodies to T. gondii anti-

gen (Toxo-IgM and Toxo-IgG) in human’s whole blood,serum or plasma. The test provides a visual qualitativeresult.22 The test was performed according to manufacturer

instructions.Confirmatory UDI ELISA test is based on the principle of

the capture of IgM and IgG with subsequent specific iden-

tification, making use of their ability to bind an antigenconjugated to peroxidase. The capture is performed usingmonoclonal antibodies bound to the solid phase. The antigen

is composed of purified and inactivated T. gondii antigens.22e

24 Results were tabulated and statistically analyzed by the chisquare test. P-values

Table 2: Toxoplasmosis suggestive/related history.

History Number of

cases

Percentage

Spontaneous abortion 112 74.7%

Previous child with congenital

anomaly

8 5.3%

Cat contact 4 2.7%

None 26 17.3%

Total 150 100%

Toxoplasma in pregnancy in Almadinah Almunawwarah 257

Thirty-two samples (21.3%) were seropositive for anti-T. gondii IgG by the rapid TOXO test and confirmed by

ELISA (Table 3). No IgM positive samples were detected byeither tests.

The highest rate of IgG seropositivity was found in the

age group 35e39 years (33.3%), whereas the lowest rate wasin the age group 20e24 years (15.4%). The youngest andoldest age groups were negative (Table 4).

Of the 112 cases with history of abortion and with chil-dren with congenital anomalies, 22 (19.6%) and 6 (75%),were IgG seropositive, respectively. Patients who owned catswere IgG negative, and the rest of the seropositive patients

had no history suggestive of toxoplasmosis (Table 5).

Table 3: Detection of anti-Toxoplasma IgG in the study cases.

Anti-Toxoplasma IgG results (both

TOXO test and ELISA)

No. of

patients

Percentage

IgG positive 32 21.3%

IgG negative 118 78.7%

Total 150 100%

Table 4: IgG seropositivity according to age groups.

Age group No. of patients IgG positive Percentage

15e19 years 11 0 0%*

20e24 years 26 4 15.4%25e29 years 49 9 18.4%

30e34 years 28 8 28.6%

35e39 years 27 9 33.3%40e44 years 7 2 28.6%

45e49 years 2 0 0%*

*Statistically significant P < 0.05.

Table 5: Correlation between IgG seropositivity and toxo-

plasmosis suggestive history.

History No. of

cases

No. of IgG

positive cases

Percentage

%

Previous abortion 112 22 19.6

Previous child with

congenital anomaly

8 6 75*

Cat contact at home 4 0 0

None 26 4 15.4

*Statistically significant P < 0.05.

Discussion

In this study, a rapid, inexpensive serodiagnostic test (onestep Toxoplasma-IgM/IgG test, InTec) was used. This test

was simple to perform in only 15 min without specialequipment or experienced personnel.24e27 The sensitivity andspecificity of the rapid tests were similar to those of the

confirmatory ELISA anti-T. gondii IgG and IgM kits,which are expensive, require specialized lab facilities andcannot be used in field studies. Given the identical results

of both methods,26,27 the rapid immunochromatographictest appears to be more suitable in toxoplasmosisscreening, especially in large scale-studies if conducted overa long period.

In the current study, IgG seroprevalence rate among thestudy subjects in Almadinah Almunawwarah was 21.3%.Compared to rates previously reported from other KSA

cities, this rate is found to be lower than those of Abha;31.6%28 and Makkah; 35.6% and 29.4%, in 2002 and 2006,respectively.6,29 However, it is much higher than the rates

reported from Hail,8 in which IgG seroprevalence was9.8% and IgM seroprevalence was 0.6% among pregnantwomen. It is noteworthy that, in the latter study, the

pregnant women tested were mostly healthy with normalpregnancies, contrary to the patients of the current study.Additionally, in 2015, another study with higherseropositivity rates was conducted in Riyadh, where

ELISA results during pregnancy revealed that theprevalence of T. gondii IgG and IgM antibodies was 32.5%and 6.4%, respectively.30

Most recently, in Makkah, a study reported that sero-prevalence of IgG was 21.2% and that of IgM was 1.2% in agroup of pregnant women with history of previous abor-

tion.31 This seems to be very near to the findings of the

Table 1: Study cases by age groups.

Age group No. of cases Percentage

15e19 years 11 7.3%

20e24 years 26 17.3%

25e29 years 49 32.7%

30e34 years 28 18.7%35e39 years 27 18%

40e44 years 7 4.7%

45e49 years 2 1.3%Total 150 100%

current study, perhaps due to similarity of the selected

group of patients, or more similar demographic and culturefactors affecting transmission of the infection in both holyIslamic cities.

The varying results from those regions of the Kingdommay be due to differences in patient numbers, demographics,history and used techniques, or the results may actually point

to more public awareness and implementation of preventivemeasures against toxoplasmosis, such as in AlmadinahAlmunawwarah.

This is the second study held in Almadinah Almu-

nawwarah. The first was made in 1992, with a seropositivityrate of 39% being detected.32 However, the study did not

N.F.A. Imam et al.258

clearly state which antibody was detected (implied to be IgG)or which diagnostic test was used and had little demographic

information and history for comparing results.In the current study, seropositivity increased with age; the

highest rate of IgG seropositivity was in the age group 35e39years (33.3%), while the youngest and oldest age groups hadno positive cases. A positive relation between increasing ageand seroprevalence of T. gondii has been already established,

due to previous longer exposure periods to the parasite. Suchpatients may retain a steady level of anti-Toxoplasma IgG inserum for years.1,29

It was reported that up to one fifth of pregnant women

with repeated abortions had anti-T. gondii IgG anti-bodies.13,16,33 In this study, a somewhat similar rate of 19.6%of cases with a history of spontaneous abortion were IgG

seropositive. However, this was not found to be significant,suggesting other abortion causes. This is not unexpectedbecause the relation between abortion and antibody

seropositivity seems to be basically linked to IgM, not IgG,titers.33e35

However, in this study, a significant relation was foundbetween IgG positive patients and history of having children

with congenital anomalies. This may incriminate toxoplas-mosis in these cases.

Furthermore, in the current study, there were no signifi-

cant associations between Toxoplasma seroprevalence andthe risk factor of having cats at home. This may indicate therising public awareness of the role of cats in transmission,6

leading to more vaccination of these pets againsttoxoplasmosis. This is in accordance with a study inMakkah, where there was no relation between

seropositivity and cat ownership.29

Generally speaking, variations in seropositivity results areexpected worldwide because of different diagnostic methodson diverse patient categories with variable obstetric his-

tory.34e36 Moreover, many risk factors, such as cat contact,handling or eating raw or undercooked meat and drinkingunfiltered water are known to have an influence on T.

gondii transmission.1 The differences in results of studies inour region are likely to stem from religious beliefs andcultural habits.29

Conclusions

Toxoplasmosis remains a problem among pregnantwomen, especially those with a history of abortion and

children with congenital anomalies. Large-scale studies areneeded to determine the exact impact it has on pregnantwomen in Almadinah Almunawwarah, involving detailed

history to highlight relevant environmental and culturalfactors. Additionally, there is a need for public awarenessprograms on toxoplasmosis within a comprehensive control

strategy.The similarity of the results obtained in this study by the

rapid test and ELISA suggests that the former is a preferred

diagnostic tool for routine testing in clinics and field settings.The rapid test is accurate, relatively inexpensive, sensitive,specific, faster and simpler than ELISA. However, serolog-ical screening should be offered only to pregnant women

considered to be at risk for primary toxoplasmosis.

Conflicts of interest

We have no conflicts of interest to declare.

Authors’ contributions

NI initiated the research idea. All authors contributed tostudy design, data collection, result analysis, draft writing,proofreading and revision. NI and EA carried out the labtests. AA had a major contribution in interpretation and

analysis of clinical data.

References

1. Remington JS, McLeod R, Thulliez P, Desmonts G. In:

Remington JS, Klein J, editors. Toxoplasmosis, infectious dis-

eases of the fetus and newborn infant. 5th ed. Philadelphia, PA:

WB Saunders; 2001. p. 205.

2. Robert-Gangneux F, Murat JB, Fricker-Hidalgo H, Brenier-

PinchartMP,Gangneux JP, PellouxH. The placenta: a main role

in congenital toxoplasmosis?Trends Parasitol 2011; 27: 530e536.3. Philip-Ephraim EE, Charidimou A, Williams E, Kajogbola G.

Stroke-like presentation of cerebral toxoplasmosis: two HIV-

infected cases. Cerebrovasc Dis Extra 2015; 5(1): 28e30.

4. Bahador S, Samaneh AK. Severe congenital toxoplasmosis: a

case report and strain characterization. Case Rep Infect Dis

2015851085. http://dx.doi.org/10.1155/2015/851085. 3 pages.

5. El Hady HM. Toxoplasmosis among pregnant women in Abha,

Saudi Arabia. J Egypt Soc Parasitol 1991; 21(3): 811e815.

6. Ghazi HO, Telmesani AM, Mahomed MF. TORCH agents in

pregnant Saudi women. Med Princ Pract 2002; 11(4): 180e182.

7. Mohammad HIAT, Balaha MH, Moghannum MS. Toxoplas-

mosis among the pregnant women attending a Saudi maternity

hospital: seroprevalence and possible risk factors. Ann Trop

Med Parasitol 2010; 104: 493e504.

8. Ashankyty IM. Seroprevalence of Toxoplasma gondii among

pregnant women visiting maternity hospital in Hail, KSA. Life

Sci J 2014; 11(8): 355e359.

9. L’Ollivier C, Wallon M, Faucher B, Piarroux R, Peyron F,

Franck J. Comparison of mother and child antibodies that

target high-molecular-mass Toxoplasma gondii antigens by

immunoblotting improves neonatal diagnosis of congenital

toxoplasmosis. Clin Vaccine Immunol 2012; 19: 1326e1328.10. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 2004; 363:

1965e1976.

11. Abdalla KF, el Fakahany AF, Arafa MA, Salama MM,

Morsy TA. Congenital toxoplasmosis among premature infants

with different clinical pictures in Saudi Arabia. J Egypt Soc

Parasitol 1994; 24(3): 643e648.

12. Montoya JG, Remington JS. Management of Toxoplasma

gondii infection during pregnancy. Clin Infect Dis 2008; 47:

554e566.

13. Rorman E, Zamir CS, Rilkis I, Ben-David H. Congenital

toxoplasmosis-prenatal aspects of Toxoplasma gondii infection.

Reprod Toxicol 2006; 21(4): 458e472.

14. Furtado JM, Smith JR, Belfort R, Gattey D, Winthrop KL.

Toxoplasmosis: a global threat.JGlob InfectDis 2011; 3: 281e284.

15. Jones JL, Dubey JP. Foodborne toxoplasmosis. Clin Infect Dis

2012; 55(6): 845e851.

16. QM1 Kong, Lu SH, Tong QB, Lou D, Chen R, Zheng B,

Kumagai T, Wen LY, Ohta N, Zhou XN. Loop-mediated

isothermal amplification (LAMP): early detection of Toxo-

plasma gondii infection in mice. Parasit Vect 2012; 3(5): 2e7.

17. Huang X, Xuan X, Hirata H, Yokoyama N, Xu L, Suzuki N,

Igarashi I. Rapid immunochromatographic test using

http://refhub.elsevier.com/S1658-3612(16)30015-4/sref1http://refhub.elsevier.com/S1658-3612(16)30015-4/sref1http://refhub.elsevier.com/S1658-3612(16)30015-4/sref1http://refhub.elsevier.com/S1658-3612(16)30015-4/sref1http://refhub.elsevier.com/S1658-3612(16)30015-4/sref2http://refhub.elsevier.com/S1658-3612(16)30015-4/sref2http://refhub.elsevier.com/S1658-3612(16)30015-4/sref2http://refhub.elsevier.com/S1658-3612(16)30015-4/sref2http://refhub.elsevier.com/S1658-3612(16)30015-4/sref3http://refhub.elsevier.com/S1658-3612(16)30015-4/sref3http://refhub.elsevier.com/S1658-3612(16)30015-4/sref3http://refhub.elsevier.com/S1658-3612(16)30015-4/sref3http://dx.doi.org/10.1155/2015/851085http://refhub.elsevier.com/S1658-3612(16)30015-4/sref5http://refhub.elsevier.com/S1658-3612(16)30015-4/sref5http://refhub.elsevier.com/S1658-3612(16)30015-4/sref5http://refhub.elsevier.com/S1658-3612(16)30015-4/sref6http://refhub.elsevier.com/S1658-3612(16)30015-4/sref6http://refhub.elsevier.com/S1658-3612(16)30015-4/sref6http://refhub.elsevier.com/S1658-3612(16)30015-4/sref7http://refhub.elsevier.com/S1658-3612(16)30015-4/sref7http://refhub.elsevier.com/S1658-3612(16)30015-4/sref7http://refhub.elsevier.com/S1658-3612(16)30015-4/sref7http://refhub.elsevier.com/S1658-3612(16)30015-4/sref7http://refhub.elsevier.com/S1658-3612(16)30015-4/sref8http://refhub.elsevier.com/S1658-3612(16)30015-4/sref8http://refhub.elsevier.com/S1658-3612(16)30015-4/sref8http://refhub.elsevier.com/S1658-3612(16)30015-4/sref8http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref9http://refhub.elsevier.com/S1658-3612(16)30015-4/sref10http://refhub.elsevier.com/S1658-3612(16)30015-4/sref10http://refhub.elsevier.com/S1658-3612(16)30015-4/sref10http://refhub.elsevier.com/S1658-3612(16)30015-4/sref11http://refhub.elsevier.com/S1658-3612(16)30015-4/sref11http://refhub.elsevier.com/S1658-3612(16)30015-4/sref11http://refhub.elsevier.com/S1658-3612(16)30015-4/sref11http://refhub.elsevier.com/S1658-3612(16)30015-4/sref11http://refhub.elsevier.com/S1658-3612(16)30015-4/sref12http://refhub.elsevier.com/S1658-3612(16)30015-4/sref12http://refhub.elsevier.com/S1658-3612(16)30015-4/sref12http://refhub.elsevier.com/S1658-3612(16)30015-4/sref12http://refhub.elsevier.com/S1658-3612(16)30015-4/sref13http://refhub.elsevier.com/S1658-3612(16)30015-4/sref13http://refhub.elsevier.com/S1658-3612(16)30015-4/sref13http://refhub.elsevier.com/S1658-3612(16)30015-4/sref13http://refhub.elsevier.com/S1658-3612(16)30015-4/sref14http://refhub.elsevier.com/S1658-3612(16)30015-4/sref14http://refhub.elsevier.com/S1658-3612(16)30015-4/sref14http://refhub.elsevier.com/S1658-3612(16)30015-4/sref15http://refhub.elsevier.com/S1658-3612(16)30015-4/sref15http://refhub.elsevier.com/S1658-3612(16)30015-4/sref15http://refhub.elsevier.com/S1658-3612(16)30015-4/sref16http://refhub.elsevier.com/S1658-3612(16)30015-4/sref16http://refhub.elsevier.com/S1658-3612(16)30015-4/sref16http://refhub.elsevier.com/S1658-3612(16)30015-4/sref16http://refhub.elsevier.com/S1658-3612(16)30015-4/sref16http://refhub.elsevier.com/S1658-3612(16)30015-4/sref17http://refhub.elsevier.com/S1658-3612(16)30015-4/sref17

Toxoplasma in pregnancy in Almadinah Almunawwarah 259

recombinant SAG2 for detection of antibodies against Toxo-

plasma gondii in cats. J Clin Microbiol 2004; 42: 351e353.

18. Villard O, Breit L, Cimon B, Franck J, Fricker-Hidalgo H,

Godineau N, Houze S, Paris L, Pelloux H, Villena I,

Candolfi E. Comparison of four commercially available avidity

tests for Toxoplasma gondii-specific IgG antibodies. Clin Vac-

cine Immunol 2013; 20(2): 197e204.19. Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP. Moving towards

an integrated approach to molecular detection and identifica-

tion of Toxoplasma gondii. Parasitology 2010; 137: 1e11.20. Paquet C, Yudin MH. Toxoplasmosis in pregnancy: prevention,

screening, and treatment. J Obstet Gynaecol 2013; 35: 78e81.

21. Gras L, Gilbert RE, Wallon M, Peyron F, Cortina-Borja M.

Duration of the IgM response in women acquiring Toxoplasma

gondiiduringpregnancy: implications for clinical practice andcross-

sectional incidence studies. Epidemiol Infect 2004; 132: 541e548.

22. Gibbs J. Selecting the detection systemdColorimetric, fluorescent,

luminescent methods. Available online: http://csmedia2.corning.

com/LifeSciences/media/pdf/elisa5.pdf [accessed 28.04.15].

23. Calderar A, Peruzzi S, Piccolo G, Gorrini C, Montecchini S,

Rossi S, Chezzi C, Dettori G. Laboratory diagnosis of Toxo-

plasma gondii infection. Int J Med Sci 2009; 6(3): 135e136.24. Béla SR, Oliveira Silva DA, Cunha-Júnior PCP, Chaves-

Borges FA, Reis de Carvalho F, Carrijo de Oliveira T,

Mineo JR. Use of SAG2A recombinant Toxoplasma gondii

surface antigen as a diagnostic marker for human acute toxo-

plasmosis: analysis of titers and avidity of IgG and IgG1 anti-

bodies. Diagn Microbiol Infect Dis 2008; 62: 245e254.

25. Jin S, Chang ZY, Ming X, Min CL, Wei H, Sheng LY,

Hong GX. Fast Dipstick dye immunoassay for detection of

immunoglobulin G (IgG) and IgM antibodies of human toxo-

plasmosis. Clin Diagn Lab Immunol 2005; 12(1): 198e201.

26. Jabbar SH, Haider FG, Abid Al-Razaq HA. Evaluation of

rapid Chromatographic immunoassay with latex agglutination

test and ELISA for diagnosis of human toxoplasmosis. J Fac

Med Baghdad 2010; 4: 469e470.27. Wang YH, Li XR, Wang GX, Yin H, Cai XP, Fu BQ,

Zhang DL. Development of an immunochromatographic strip

for the rapid detection of Toxoplasma gondii circulating anti-

gens. Parasitol Int 2011; 60(1): 105e107.

28. Aqeely H, El-Gayar EK, Perveen Khan D, Najmi A, Alvi A,

Bani I, Mahfouz MS, Abdalla SE, Elhassan IM. Seroepidemi-

ology of Toxoplasma gondii amongst pregnant women in Jazan

Province, Saudi Arabia. J Trop Med 2014913950. http://

dx.doi.org/10.1155/2014/913950.

29. Al-Harthi SA, Jamjoom MB, Ghazi HO. Seroprevalence of

Toxoplasma gondii among pregnant women in Makkah, Saudi

Arabia.UmmAl-QuraUniv. J SciMed Eng 2006; 18(2): 217e227.

30. Alghamdi J, Elamin MH, Alhabib S. Prevalence and genotyp-

ing of Toxoplasma gondii among Saudi pregnant women in

Saudi Arabia. Saudi Pharm J 2015 [in press].

31. Khalil M, Adil B, Narjes D, Suzan B, Al Bagir M, Ali AM,

Ahmad B. Detection of Toxoplasma gondii infection and asso-

ciated risk factors among pregnant women in Makkah Al

Mukarramah, Saudi Arabia. Asian Pac J Trop Dis 2016; 6(2):

113e119.

32. Ikram MH. Antibody to Toxoplasma gondii among pregnant

women in Medina Munawarah. J Pak Med Assoc 1992; 42(2):

44e45.

33. Halonen SK, Weiss LM. Toxoplasmosis. Handb Clin Neurol

2013; 114: 125e145.

34. Cenci-Goga BT, Rossitto PV, Sechi P, McCrindle CM,

Cullor JS. Toxoplasma in animals, food, and humans: an old

parasite of new concern. Food Borne Pathog Dis 2011; 8(7):

751e762.35. Siddiqui N, Shujatullah F, Khan HM, Rabbani T, Khan PA.

IgG avidity antibodies against Toxoplasma gondii in high risk

females of reproductive age group in India. Korean J Parasitol

2014; 52(5): 487e491.36. Agmas B, Tesfaye R, Koye DN. Seroprevalence of Toxoplasma

gondii infection and associated risk factors among pregnant

women in Debre Tabor, Northwest Ethiopia. BMC Res Notes

2015; 8: 107. http://dx.doi.org/10.1186/s13104-015-1083-2.

How to cite this article: Imam NFA, Azzam EAA, AttiaAA. Seroprevalence of Toxoplasma gondii amongpregnant women in Almadinah Almunawwarah KSA. JTaibah Univ Med Sc 2016;11(3):255e259.

http://refhub.elsevier.com/S1658-3612(16)30015-4/sref17http://refhub.elsevier.com/S1658-3612(16)30015-4/sref17http://refhub.elsevier.com/S1658-3612(16)30015-4/sref17http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref18http://refhub.elsevier.com/S1658-3612(16)30015-4/sref19http://refhub.elsevier.com/S1658-3612(16)30015-4/sref19http://refhub.elsevier.com/S1658-3612(16)30015-4/sref19http://refhub.elsevier.com/S1658-3612(16)30015-4/sref19http://refhub.elsevier.com/S1658-3612(16)30015-4/sref20http://refhub.elsevier.com/S1658-3612(16)30015-4/sref20http://refhub.elsevier.com/S1658-3612(16)30015-4/sref20http://refhub.elsevier.com/S1658-3612(16)30015-4/sref21http://refhub.elsevier.com/S1658-3612(16)30015-4/sref21http://refhub.elsevier.com/S1658-3612(16)30015-4/sref21http://refhub.elsevier.com/S1658-3612(16)30015-4/sref21http://refhub.elsevier.com/S1658-3612(16)30015-4/sref21http://csmedia2.corning.com/LifeSciences/media/pdf/elisa5.pdfhttp://csmedia2.corning.com/LifeSciences/media/pdf/elisa5.pdfhttp://refhub.elsevier.com/S1658-3612(16)30015-4/sref23http://refhub.elsevier.com/S1658-3612(16)30015-4/sref23http://refhub.elsevier.com/S1658-3612(16)30015-4/sref23http://refhub.elsevier.com/S1658-3612(16)30015-4/sref23http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref24http://refhub.elsevier.com/S1658-3612(16)30015-4/sref25http://refhub.elsevier.com/S1658-3612(16)30015-4/sref25http://refhub.elsevier.com/S1658-3612(16)30015-4/sref25http://refhub.elsevier.com/S1658-3612(16)30015-4/sref25http://refhub.elsevier.com/S1658-3612(16)30015-4/sref25http://refhub.elsevier.com/S1658-3612(16)30015-4/sref26http://refhub.elsevier.com/S1658-3612(16)30015-4/sref26http://refhub.elsevier.com/S1658-3612(16)30015-4/sref26http://refhub.elsevier.com/S1658-3612(16)30015-4/sref26http://refhub.elsevier.com/S1658-3612(16)30015-4/sref26http://refhub.elsevier.com/S1658-3612(16)30015-4/sref27http://refhub.elsevier.com/S1658-3612(16)30015-4/sref27http://refhub.elsevier.com/S1658-3612(16)30015-4/sref27http://refhub.elsevier.com/S1658-3612(16)30015-4/sref27http://refhub.elsevier.com/S1658-3612(16)30015-4/sref27http://dx.doi.org/10.1155/2014/913950http://dx.doi.org/10.1155/2014/913950http://refhub.elsevier.com/S1658-3612(16)30015-4/sref29http://refhub.elsevier.com/S1658-3612(16)30015-4/sref29http://refhub.elsevier.com/S1658-3612(16)30015-4/sref29http://refhub.elsevier.com/S1658-3612(16)30015-4/sref29http://refhub.elsevier.com/S1658-3612(16)30015-4/sref30http://refhub.elsevier.com/S1658-3612(16)30015-4/sref30http://refhub.elsevier.com/S1658-3612(16)30015-4/sref30http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref31http://refhub.elsevier.com/S1658-3612(16)30015-4/sref32http://refhub.elsevier.com/S1658-3612(16)30015-4/sref32http://refhub.elsevier.com/S1658-3612(16)30015-4/sref32http://refhub.elsevier.com/S1658-3612(16)30015-4/sref32http://refhub.elsevier.com/S1658-3612(16)30015-4/sref33http://refhub.elsevier.com/S1658-3612(16)30015-4/sref33http://refhub.elsevier.com/S1658-3612(16)30015-4/sref33http://refhub.elsevier.com/S1658-3612(16)30015-4/sref34http://refhub.elsevier.com/S1658-3612(16)30015-4/sref34http://refhub.elsevier.com/S1658-3612(16)30015-4/sref34http://refhub.elsevier.com/S1658-3612(16)30015-4/sref34http://refhub.elsevier.com/S1658-3612(16)30015-4/sref34http://refhub.elsevier.com/S1658-3612(16)30015-4/sref35http://refhub.elsevier.com/S1658-3612(16)30015-4/sref35http://refhub.elsevier.com/S1658-3612(16)30015-4/sref35http://refhub.elsevier.com/S1658-3612(16)30015-4/sref35http://refhub.elsevier.com/S1658-3612(16)30015-4/sref35http://dx.doi.org/10.1186/s13104-015-1083-2

Seroprevalence of Toxoplasma gondii among pregnant women in Almadinah Almunawwarah KSAIntroductionMaterials and MethodsResultsDiscussionConclusionsConflicts of interestAuthors' contributionsReferences