Abstract
Bad obstetric history (BOH) is associated with social and psychological impacts on society worldwide. The causes of BOH may be genetic, hormonal, abnormal maternal immune response, and maternal infection. In women with bad obstetric history (BOH), Toxoplasma (T) IgG high rate has been reported for Nepal (55.2%), while high (42.5%) and lowest (6.97%) active toxoplasma infections has been reported for India. In Arab countries, IgG and IgM higher and lowest seroprevalence rates were for Iraq. The higher susceptibility rates for Rubella in Arab countries excluding Iraq were reported in Morocco (83.4%), Sudan (34.7%), Qatar (25.1%), and Tunisia (20.3%). The lowest susceptibility was reported for Saudi Arabia (6.7%). In Iraq, studies indicate a high susceptibility rates in Thi Qar (98.05%), Kirkuk (91%), Baghdad (79%), and Waset (45.7%). The lowest susceptibility rates were reported for Diyala (0%) in women with previous abortion, and 3.9% in pregnant women without history of BOH.
Key words: TORCH; Toxoplasma; Rubella; CMV; Cytomegalovirus; HSV
Introduction
Bad obstetric history (BOH) implies previous unfavorable fetal outcome in terms of two or more consecutive spontaneous abortions, history of intrauterine fetal death, intrauterine growth retardation, stillbirth, early neonatal death, and/or congenital anomalies [1]. The causes of BOH may be genetic, hormonal, abnormal maternal immune response, and maternal infection [2,3].
TORCH Complex:
The TORCH infections can lead to severe fetal anomalies or even fetal loss. They are a group of viral, bacterial, and protozoan infections that gain access to the fetal bloodstream transplacentally via the chorionic villi. Hematogenous transmission may occur at any time during gestation or occasionally at the time of delivery via maternal-to-fetal transfusion [4]. Primary infections caused by TORCH-Toxoplasma gondii, Rubella virus, cytomegalovirus (CMV), and herpes simplex virus (HSV)-are the major causes of BOH [5]. These infections usually occur before the woman realizes that she is pregnant or seeks medical attention. The primary infection is likely to have a more important effect on fetus than recurrent infection and may cause congenital anomalies, spontaneous abortion, intrauterine fetal death, intrauterine growth retardation, prematurity, stillbirth, and live born infants with the evidence of disease [6]. Most of the TORCH infections cause mild maternal morbidity but have serious fetal consequences [7]. The ability of the fetus to resist infectious organisms is limited and the fetal immune system is unable to prevent the dissemination of infectious organisms to various tissues [8]. TORCH infections in the mother are transmissible to fetus in the womb or during the birth process and cause a cluster of symptomatic birth defects. Many sensitive and specific tests are available for serological diagnosis of TORCH complex [9]; however, ELISA test is more routinely used for its sensitivity. An attempt is being made to find out the correlation of TORCH infection during pregnancy in the Iraqi population. Toxoplasma gondii is an obligate intracellular protozoan parasite, which is linked to one of the most prevalent chronic infections affecting one third of the world’s human population [10]. The infection is characterized by non-specific symptoms with the consequent formation of cysts that may remain in latent form in many organs [11]. Primary infection is usually subclinical but the infection hazard is its occurrence during pregnancy. There are four groups of individuals in whom the diagnosis of toxoplasmosis is most critical: a) pregnant women who acquire their infection during gestation, b) fetuses, c) newborns who are congenitally infected, immunocompromised patients, and d) those with chorioretinitis [12-14]. Although congenital toxoplasmosis is not a nationally reportable disease in Iraq, it represents a health care problem. Reported studies indicated an estimated 400 to 4,000 cases occur in the U.S. each year [11,15,16]. The overall prevalence and incidence varies in different communities and contributes significantly to heavy morbidity [10]. Congenital toxoplasmosis mainly results from a primary infection acquired during pregnancy [17], but not from the reactivation of a latent infection in immunocompetent pregnant women [18]. However, it is believed that latent toxoplasmosis could reactivate and cause a congenital transmission of the parasite to infants who then become infected in utero [19]. Countries with high disease prevalence have instituted successful secondary prevention programs via widespread maternal serologic screening [20], but universal maternal serologic screening for toxoplasmosis is not currently recommended in most of countries [21-24]. Instead, current practice suggests maternal serological screening when abnormal fetal findings or presence of infertility problem indicate possible infection [22]. ELISA methods is commonly performed in many countries to detect anti-toxoplasma antibodies [25]. ELISA results are generally well accepted by clinicians because of their excellent sensitivities and specificities, the rapid availability of results, and the relatively low costs of the tests. It is important to understand that a single serologic test is not enough for the diagnosis of toxoplasmosis [26]. In worldwide, commercial test kits for Toxoplasma-specific IgG and IgM antibodies are readily available. The presence of IgM antibodies is not always an indication of a recent infection since IgM maybe present for many months [27,28]. Misdiagnosis of recent infections may be as a result of the presence of specific T. gondii IgM antibodies in the chronic stage of an infection, or false-positive IgM positivity [17,29]. IgM test results are difficult to interpret and the reliability of test kits is largely dependent upon other factors. A negative IgM with a positive IgG result can indicate infection at least 1 year before. A positive IgM result may indicate more recent infection or may also be a false positive reaction [25]. Currently worldwide, there is no systematic screening of pregnant women to detect seroconversion during gestation and most clinicians make decisions depending on result of single serum sample. This approach is not effective to detect toxoplasma infections during pregnancy, thus monthly serological screening for pregnant women is the recommended approach [30]. The presence of elevated levels of Toxoplasma specific IgG antibodies indicates infection has occurred at some point, but does not distinguish between an infection acquired recently and one acquired in the distant past. In acute infection, IgG and IgM antibodies generally rise within 1 to 2 weeks of infection [31]. Given the potential for false-positive results, the true value of IgM testing is in ruling out the presence of acute infection. In other words, negative IgM results are reassuring, whereas positive results should be interpreted carefully, confirmed in a toxoplasmosis reference laboratory, and followed by serial titers at least 3 weeks apart [12,28,32]. There are different Toxoplasma seropositivity reports from all over the world. The population of Turkish childbearing age women has the seropositivity of T. gondii as 1.34% for IgM and 24.6% for IgG [33]. In Maracaibo, Venezuela the overall prevalence of toxoplasmosis was 33%, while 18.2% were positive IgM [34]. In Qatar among 823 women of childbearing age, the T. gondii IgG and IgM was 35.1% and 5.2% respectively [35]. Sixty-five studies [3,33,36-97] characterizing the prevalence of maternal infections with T. gondii in developing and developed countries and fifty-nine [35,98-155] studies in Arab countries (30 studies reported for Iraq) were identified. The features and results of these studies are summarized in Tables I and II.The majority of studies had small sample sizes, between 0– 4112 subjects. Most of these studies were conducted in antenatal clinics, hospitals, health care facilities or prenatal clinics. The remaining studies (3.3%) were community-based and the study setting was not specified in 7.4% of the studies. The most commonly used test was ELISA, which is the gold standard for T. gondii analysis. The median of IgG Toxoplasma prevalence was 38.5% [64] for Bangladesh. IgG high rate of detection was reported for Brazil [50] (75%, 832 pregnant women), while the lowest rate was for Thailand [38] (5.3%, 831 pregnant women). IgM lowest rate reported for China [49] (0%, 235 pregnant women) and Vietnam [59] (0%, 300 pregnant women), while the highest rate reported for Ghana [87] (76.1%, 159 pregnant women). In women with bad obstetric history (BOH), IgG high rate was reported for Nepal [62] (55.2%, 345 BOH) and the lowest one was that reported by Natu et al [74] (19.44%, 499 BOH). IgM in BOH high rate was reported for India [36] (42.5%, 200 BOH), while the highest one for India also [91] (6.97%, 86 BOH). In Arab countries, the median of IgG prevalence was 41.9% which was reported for Sudan [144]. IgG highest rate of detection reported for Iraq [132] (94%, 54 pregnant women) Bahrain [137] (15.8%, 146 Pregnant women), while the corresponding values for IgM were 55.5% (Iraq, 180 pregnant women) [129] and 2.8% (Egypt, 323 pregnant women) [153] respectively. Concerning BOH, IgG ranges between 77.1% (Iraq,122 BOH) [114] and 6.84% (Iraq, 190 BOH) [130], while the range of IgM was between 58% (Iraq, 50 BOH) [127] and 0.97% (Iraq, 310 BOH) [104].
Article |
Location, setting of study |
Type, Duration |
Population |
Results |
Wanachiwanawin et al [38] |
Thailand, antenatal clinic |
Cross sectional , 2 years |
831 Pregnant women |
5.3% IgG, IgM positive in 4.5%
of IgG positive |
Lopes et al [39] |
Brazil, antenatal clinic |
Cross sectional, 7 months |
492 Pregnant women |
49.2% IgG, IgM 1.2% of IgG
positive |
Varella et al [40] |
Brazil, Hospital |
Cross-sectional, 7 years |
41112 Pregnant women |
0.48% seroprevalence |
Khurana et al [41] |
India, antenatal clinic |
Cross sectional,
No information |
300 Pregnant women |
15.3% IgG, 3% IgM |
Vaz et al [42] |
Brazil, No information |
Cross-sectional, 15 months |
20389 Pregnant women |
53.3% IgG, 3.26% IgM |
Alvarado-Esquivel et al [43] |
Mexico, Rural |
Community based, |
439 Pregnant women |
8.2% IgG, 2.3% IgM |
Sakikawa M et al [44] |
Japan, antenatal clinic |
All cases screening, 7.5 years |
4466 Pregnant women |
10.3% seroprevalence, 0.25%
primary infection |
Maggi et al [45] |
Albania, General outpatient
centre |
Screening, 6 months |
498 Pregnant women |
48.6% IgG, IgM 1.3% of IgG
positive
|
Sen MR et al [46] |
India, Hospital |
Descriptive case control, 2
years |
380 pregnant women |
19.4% IgM |
Sarkar et al [47] |
India, antenatal clinic |
Descriptive case control, 10
months |
105 Pregnant women |
49.52% IgG, 21.9% IgM |
Barbosa et al [48] |
Brazil, Maternity hospital |
Cross-sectional, 10 months |
190 Pregnant women |
66.3% IgG, 0.53% IgM |
Liu et al [49] |
China, antenatal clinic |
Cross-sectional |
235 Pregnant women |
10.6% IgG, 0% IgM |
Ribeiro et al [50] |
Brazil, PHC |
Cross sectional, 3.5 years |
832 Pregnant women |
75.1% IgG, 2% IgM |
Rosso et al [37] |
Colombia, Healthcare facility |
Cross-sectional, 5 months |
955 Pregnant women |
45.8% IgG, 2.8% IgM |
Abdi et al [51] |
Iran, |
Cross-sectional, |
553 Pregnant women |
44.8% IgG |
Mostavi N [52] |
Iran, Survey |
Cross-sectional, 1 year |
217 Child bearing age |
47.5% seroprevalence (IgG) |
Hajsoleimani [53] |
Iran, PHC |
Cross-sectional, |
500 Pregnant women |
37.2% IgG, 1.4% IgM |
Ndiaye et al [54] |
Senegal, Hospital |
Cross-sectional, 1 year |
109 Pregnant Women |
22% IgG, 3% IgM |
Spalding et al [55] |
Brazil, PHC |
Cross-sectional, 18 months |
2128 Pregnant women |
71.5% IgG, 3.6% IgM |
Castilho-Pelloso et al [56] |
Brazil, Public health care |
Observational Retrospective,
3 years |
290 Pregnant women |
1.07% IgM |
Sharifi-Mood et al [57] |
Iran, Hospital |
Cross sectional, |
200 Pregnant women |
27% serpositive |
Ndir et al [58] |
Senegal, Health centre |
Case control, 6 months |
70 Pregnant & 70
Abortion cases |
37.1% in pregnant, 40% in
abortion |
Buchy et al [59] |
Vietnam, |
Cross-sectional, |
300 Pregnant women |
11.2% IgG, 0% IgM |
Akoijam et al [60] |
India, Antenatal clinic |
Cross-sectional, 1 year |
503 Pregnant women |
41.75% seroprevalence |
Mahdi et al [61] |
Iran, Antenatal clinic |
Cross-sectional, |
245 Pregnant women |
49.2% seroprevalence |
Rai et al [62] |
Nepal, Antenatal clinic |
Cross-sectional, 2 years |
345 BOH |
55.2% seroprevalence |
Chintana et al [63] |
Thailand, Antenatal Clinic |
Cross-sectional, 6 months |
1200 Pregnant women |
13.2% IgG |
Ashrafunnessa et al [64] |
Bangladesh, Antenatal clinic |
Cross-sectional |
286 Pregnant women |
38.5% IgG |
Zhang et al [65] |
China |
Cross-sectional |
1250 Pregnant women |
7.28% seroprevalence |
Sroka et al [66] |
Brazil, Hospital |
Cohort, 10 weeks |
963 Pregnant women |
68.6% IgG, 0.5% IgM |
Zhang et al [67] |
China, antenatal clinic |
Cross-sectional |
4126 Pregnant women |
3.38% IgM |
Gonzalez-Morales et al [68] |
Cuba, Health centres |
Cross-sectional, 2 years |
3913 Pregnant women |
70.9% seroprevalence |
Galvan Ramirez et al [69] |
Mexico, Hospital |
Case control |
350 High risk pregnancy |
34.9% IgG, 20.7% IgM |
Lelong et al [70] |
Madagascar, |
|
599 Pregnant women |
83.5% seroprevalence |
Sun et al [71] |
China, hospital |
Cross sectional |
1211 Pregnant women |
39.14% IgG, 4.21% IgM |
Martinez Sanchez et al [72] |
Cuba, Community survey |
Cross sectional, 6 months |
362 Pregnant women |
71% seroprevalence |
Bari et al [73] |
India, antenatal clinic |
Cross sectional |
302 Pregnant women |
46% IgG, 27.7% IgM |
Natu et al [74] |
|
Case control |
499 BOH |
19.44% seroprevalence |
Bittencourt [75] |
Brazil, Public health services |
Cross sectional, 16 months |
4022 Pregnant women |
59.8% IgG, 1.1% IgM |
Shanmugam et al [76] |
India, antenatal |
Cross sectional |
225 Pregnant women |
23.6% Seropositive |
Reis et al [77] |
Brazil, Hospital |
Cross sectional, 6 years |
10468 |
61.1% Seroprevalence |
Harma et al [78] |
Turkey, Prenatal clinic |
Cross-sectional, |
1149 Pregnant women |
60.4% IgG, 3% IgM |
Hou et al [79] |
China, Hospital |
Cross-sectional |
347 Pregnant and post
partum women |
5.5% seroprevalence. |
Doehring et al [80] |
Tanzania, Hospital |
Cross-sectional |
849 Pregnant women |
35% Seropositive |
Soto et al [81] |
Venezuela, Hospital |
Cross sectional |
7969 Pregnant women |
53.91% Seroprevalence |
Khurana et al [82]
|
India, Antenatal clinic
|
Cross-sectional
|
300 Pregnant women
|
15.33% IgG, 3% IgM
|
Ouermi et al [83]
|
Burkina Faso, Healthcare
facility
|
Cross-sectional 6 months
|
276 Pregnant women
|
27.2% IgG, 4.7% IgM
|
Zemene et al [84]
|
Ethiopia, Community based
|
Cross-sectional, 2 months
|
201 Pregnant women
|
81.1% IgG, 2.5% IgM
|
Flatt A & Shetty N [85]
|
UK, Antenatal clinic
|
Cohort, 2 years
|
5000 Pregnant women
|
17.32 % IgG
|
Surpam et al [86]
|
India, Antenatal clinic
|
Case control,
|
150 BOH
|
14.66% IgM
|
Ayi et al [87]
|
Ghana, Antenatal clinic
|
Cross-sectional, 4 months
|
159 Pregnant women
|
73.6% IgG, 76.1 IgM
|
Cvetkovic D et al [88]
|
Macedonia,
|
Retrospective, 2 years
|
235 Pregnant women
|
20.4% overall seroprevalence
|
Karabulut A et al [89]
|
Turkey, Antenatal clinic
|
Case control, 1 year
|
1102 Pregnant women
|
37% IgG, 1.4% IgM
|
Kumari N et al [1]
|
Nepal, Hospital
|
Case control, 4 months
|
12 BOH
|
50% seropositive
|
Nabi SN et al [90]
|
Bangladesh, Hospital
|
Case control, 10 months
|
111 Pregnant women
|
23.42% IgG, 0.9% IgM
|
Sadik MS et al [91]
|
India, Hospital
|
Case control, 2 years
|
86 BOH
|
20.93% IgG, 6.97% IgM
|
Akyar I [33]
|
Turkey, Hospital
|
Cross sectional, 7.5 years
|
17751 Child bearing age
|
24.6% IgG, 1.34% IgM
|
Frischknecht F et al [92]
|
Switzerland, Hospital
|
Cross sectional, 1 yr
|
723 Pregnant women
|
44.11% serpositive
|
Inagaki ADM, et al [93]
|
Brazil, Antenatal clinic
|
Cross sectional, 1 year
|
9559 Pregnant women
|
69.3% IgG, 0.4% IgM
|
Turbadkar D, et al [3]
|
India, Antenatal clinic
|
Case control, 1 year
|
380 BOH
|
42.1% IgG, 10.52% IgM
|
Linguissi LS et al [94]
|
Burkia Faso,
|
Cross sectional, 3 years
|
Pregnant women
|
20.37% IgG
|
Chopra S et al [36]
|
India, Antenatal clinic
|
Case control, 1 year
|
200 BOH
|
42.5% IgM
|
Koksaldi-Motor et al [95]
|
Turkey, Hospital
|
Cross sectional, 1 year
|
1103 Childbearing age
|
59.9% IgG
|
Vilibik-Cavlek T, et al [96]
|
Croatia, Hospital
|
Cross sectional, 5 years
|
Pregnant & non pregnant women
|
29.1% IgG, 0.25% IgM
|
Goncalves MA, et al, [97]
|
Brazil, Hospital
|
Retrospective, 2 years
|
574 Pregnant women
|
62% IgG, 3.4% IgM
|
Table I. Characteristics and results of studies reporting prevalence of maternal Toxoplasma infection.
Article |
Location, setting of study |
Type, duration of study |
Population |
Results |
Al-Ani RT [103] |
Iraq, Al- Anbar, Hospital |
Cross sectional, 6 months |
50 Pregnant women |
50% IgM |
Razzak et al [104] |
Iraq, Duhok, Hospital |
Case control, 18 months |
310 Women with BOH |
0.97% IgM |
El Mansouri et al [105] |
Morocco, Institute National
Hygiene |
Cross-sectional |
2456 Pregnant women |
50.6% seroprevalence |
Elnahas et al [106] |
Sudan, Antenatal clinic |
7 months |
487 Pregnant women |
34.1% IgG, 14.3% IgM |
Abdel-Hafez et al [107] |
Jordan, |
Case control, 1 year |
55 Aborted women
46 Pregnant women |
58.2% Aborted women, 26.1% Pregnant women |
Hammouda et al [108] |
Egypt, Hospital |
Case control, |
100 BOH |
65% seroprevalence |
Abdulmohaymen N [99] |
Iraq (Baghdad), Hospital |
Case control, 9 months |
119 Aborted women |
24.2% IgM recurrent spontaneous abortion
14.7% IgM non recurrent spontaneous abortion.
8.1% IgG recurrent spontaneous abortion
5.9% IgG non recurrent spontaneous abortion |
Salih HA [109] |
Iraq, Najaf, Hospital |
Case control |
260 Aborted women |
30.76% IgG, 11.92% IgM |
Al-Mohammad et al [110] |
Saudi Arabia, Maternity
Hospital |
Cross-sectional, 1 year |
554 Pregnant women |
51.4% IgG, 8.8 IgM |
Jasim et al [100] |
Iraq, Waset, Hospital |
Case control, 1 year |
162 Aborted women |
53.9% IgG, 54.8% IgM |
Al- Taie et al [101] |
Iraq, Mosul, Private
laboratory |
Case control, 1 year |
100 BOH |
43% IgM |
Al Seadawy MAH [111] |
Iraq, Al Muthana, Hospital |
Case control, 3 months |
81 Aborted women |
44.5% IgM |
Mousa DA [112] |
Libya, Hospital |
Case control, 6 months |
143 BOH |
44.8% IgG, 8.4% IgM |
Mahmood SH et al [113] |
Iraq, Baghdad, Public Health
Central Laboratory |
Case control, 8 months |
120 Aborted women |
39.16% IgG, 17.79% IgM |
Aziz & Drueish[114] |
Iraq, Baghdad, Hospital |
Case control |
122 Aborted women |
77.1% IgG, 58.1% IgM |
Al-Hamdani & Mahdi [115] |
Iraq, Basrah, PHC |
Case control, 8 months |
81 Habitual abortion |
18.5% seropositive |
Al-Sodany & Saleh [116] |
Iraq, Basrah, Hospital |
Case control, 8 months |
81 Habitual abortion |
81.5% seropositive |
Majeed AK [117] |
Iraq, Baghdad, |
Case control, 3 years |
260 Aborted women for IgG
259 Aborted women for IgM |
21.2% IgG35.1% IgM |
Alsaeed et al [118] |
Iraq, Al-Hila, Hospital |
Case control, 6 months |
120 Aborted women |
41.66% seropositive |
Almishhadani & Aljanabi
[119] |
Iraq, Al- Anbar, Medical
Laboratory |
Case control study, 3 years |
230 Aborted women |
58.3% IgG, 8.3% IgM |
Khudair M K [120] |
Iraq, Diala, Hospital |
Case control, 5 months |
50 Aborted women |
54% seropositive |
Hasan SF [121] |
Iraq, Karbala, Immunology
Centre |
Cross sectional, 3 months |
82 Childbearing age women |
18.3% IgG |
Ali AA [122] |
Iraq, Al- Tameem, Hospital |
Cross sectional, 1 year |
100 Pregnant women
97 BOH |
61% Seroprevalence
74.22% BOH non pregnant |
Kadir MA et al [123] |
Iraq, Kirkuk, Hospital &
PHC |
Cross sectional, 7 months |
319 Pregnant women
121 Aborted women |
36.6% seroprevalence LAT,
16.92 IgM ELISA52% LAT,
25.61% IgM ELISA |
Alkulabi R [124] |
Iraq, Najaf, Hospital |
Cross sectional study |
137 Pregnant women |
60.5% IgG, 43.7% IgM |
Yousif JJ et al [125] |
Iraq, Najaf, PHC |
Cross sectional, 3 months |
120 Pregnant women
120 Non pregnant |
40% IgG29.2% IgG |
Al-khafaji & Mohsen [126] |
Iraq, Thi Qar, Hospital |
Case control, 10 months |
74 Habitual abortion |
23% IgG, 31.1% IgM |
Alkhashab FMBA, et al
[127] |
Iraq, Mosul, Hospital |
Case control, 16 months |
50 Aborted women,
100 Pregnant women |
34% IgG, 58% IgM20% IgG,
41% IgM |
Alaa Z [128] |
Iraq, Tikrit, Hospital |
Case control, 15 months |
226 BOH |
26.1% IgG, 3.1% IgM |
Rashid KN [102] |
Iraq, Tikrit, Private
laboratory |
????? |
100 Women 15 -45 years age |
46% IgG, 32% IgM of IgG
positive cases, |
Al-Marzoqi AHM, et al
[129] |
Iraq, Babylon, Hospital |
Cross sectional, 6 months |
180 Pregnant women |
62.2% IgG, 55.5% IgM |
Hadi NJ [130] |
Iraq, Thi Qar, Hospital |
Case control |
190 Aborted women |
6.84% IgG, 12.63% IgM |
Salman YG [131] |
Iraq, Kirkuk, Hospital |
Case control, 11 months |
184 BOH |
4.84% Seropositive, 17% IgM |
Mossa HAL [132] |
Iraq, Baghdad, Hospital |
Retrospective, 2 years |
54 Pregnant women |
94% IgG, 33% IgM |
Al- Shimmery MN [133] |
Iraq, Diwanya, Hospital |
Case control, 5 months |
125 Aborted women |
45.6% IgG, 29.6% IgM |
Bouratbine A, et al [134] |
Tunisia, Hospital |
Cross sectional |
1421 community sample |
70% seroprevalence at age of
30 years |
Barkat A et al [135] |
Morocco, Hospital |
Cross sectional, 1 year |
368 Pregnant women |
44.3% IgG |
Bouhamdan SF et al [136] |
Lebanon, Hospital &
Private laboratories |
Retrospective, 1year |
3516 Female for IgG
3426 Female for IgM |
62.2% IgG6.8% IgM |
Tabbara & Saleh [137] |
Bahrain, Hospital |
Cross-sectional, 46 months |
146 Delivering women |
15.8% IgG |
Ibrahim HM et al [138] |
Egypt, Private Clinical
Laboratory |
Cross sectional, |
101 Pregnant women |
51.49% seroprevalence |
Al-Hindi & Lubbad [139] |
Palestine, Hospital |
Case control, 6 months |
312 Aborted women |
17.9% IgG, 12.8% IgM |
Abu- Madi MA, et al [35] |
Qatar, Hospital |
Cross sectional, 3 years |
847 Women > 20 yr age |
38.2% IgG, 5.1% IgM |
Gashout A, et al [140] |
Libya, Hospital |
Case control, 5 years |
692 Aborted women |
45% IgG, 17.6% IgM |
Al-Qahtani & Hassan [141] |
Saudi Arabia, Hospital |
Cross sectional, 5 months |
75 Adult female |
44% seroprevalence |
Al-Harithi SA et al [142] |
Saudi Arabia, Hospital |
Cross sectional, 6 months |
197 Pregnant women |
29.4% IgG, 5.6% IgM |
Elamin MH, et al [143] |
Sudan, Hospital |
Case control, |
94 Pregnant Aborted during
study
94 Pregnant with normal
outcome |
35.1% IgG, 15.2% IgM, 39.4%
IgG, 16.2% IgM, Overall 37.2%
IgG, 5.9% IgM |
Khalil KM, et al [144] |
Sudan, Hospital |
Case control, |
245 Pregnant women
209 Aborted women |
35.9% seroprevalence58.3%
Seroprevalence |
Mohamad K, et al [145] |
Sudan, Hospital |
Cross sectional, |
253 Childbearing age women |
73.1% IgG |
Al- Nahari AM, et al [146] |
Yemen, Central Laboratory |
Cross sectional, 2 years |
463 Pregnant women |
41.9% IgG, 11.88% IgM |
Ghazi HO, et al [147] |
Saudi Arabia, Hospital |
Cross sectional |
926 Pregnant women |
35.6% IgG |
Sellami H, et al [148] |
Tunisia, Hospital |
Cross sectional, 13 years |
40 566 Pregnant women |
39.3% seroprevalence, 1.3%
acute infection during pregnancy. |
Almogren A [149] |
Saudi Arabia, Hospital |
Retrospective, 1 year |
2176 Pregnant women |
38% IgG, 0% IgM |
Al- Hindi A, et al [150] |
Palestine, IVF centre |
Retrospective, 6 years |
1954 Women with infertility or
abortion |
7.9% IgM |
El-Gozamy BR, et al [151]
|
Egypt, Hospital
|
Cross sectional, 17 months
|
|
Rural 57.6% seroprevalence, 46.5%
Urban
|
Hussein AH, et al [152]
|
Egypt, Hospital
|
Case control,
|
152 randomly selected
individuals, 31 full term
pregnant, 38 BOH
|
IgG- 57.9%, 58.1%, 44.7%
IgM –10.5%, 6.5%, 23.7%
|
El- Deeb HK, et al (153)
|
Egypt, Hospital
|
Cross sectional
|
323 Pregnant women
|
67.5% IgG, 2.8% IgM
|
El- Ridi AM, et al, [154]
|
Egypt, Hospital
|
Case control,
|
72 BOH
|
27.8 % Seropositive
|
Jumaian NF [98]
|
Jordan, Antenatal
|
Cross sectional,17 months
|
280 Pregnant women
|
47.1 seropositive,
|
Mohammed TK [155]
|
Iraq, Baghdad, Hospital
|
Cross sectional, 6 months
|
212 Pregnant women
|
28.77% IgG, 23.8% IgM
|
Table II. Characteristics and results of studies in Arab countries reporting prevalence of maternal Toxoplasmosis infection.
Rubella virus
Rubella is a contagious viral disease caused by a togavirus and usually goes unnoticed. However, maternal infection during pregnancy may result in fetal loss or in congenital rubella syndrome (CRS) [156,157]. Infection in the first eight to ten weeks of pregnancy results in damage in up to 90% of surviving infantswhere multiple defects are common. The risk of damage declines to about 10 to 20% with infection occurring between 11 and 16 weeks gestation [158]. Fetal damage is rare with infection after 16 weeks of pregnancy, with only deafness being reported following infections up to 20 weeks of pregnancy. Some infected infants may appear normal at birth but perceptive deafness may be detected later [157,158]. Before the introduction of Rubella immunisation, Rubella was commonly prevalent in children, and more than 80% of adults had evidence of previous rubella infection [159] Rubella infection of a pregnant woman may have devastating effects on the developing fetus and once congenital infection occurred there is no availability of treatment for the foetus. Thus the mainstay of prevention is the universal immunization of all infants and identification and immunization of women at risk [156]. Fetal infection is acquired hematogenously, and the rate of transmission varies with the gestational age at which maternal infection occurs, with higher frequency in first trimester [160]. Periconceptual maternal infection does not seem to increase the risk of CRS [160]. Maternal immunity, either after vaccination or naturally derived, is generally protective against intrauterine rubella infection [162,163]. However, there have been cases of CRS after maternal reinfection [163]. Therefore, CRS should always be considered in a fetus or neonate with a clinical picture suggestive of congenital infection [162]. It should be noted that no case of CRS has been reported when maternal reinfection occurred after 12 weeks of pregnancy [164]. Fifty- nine studies (Tabl. III) characterizing the epidemiology of maternal rubella were identified mostly for low and middle income countries [1,3,36,89-97,165-211] and 19 studies (Tabl. IV) for Arab countries [35,100,101,129-131,140,150,212-221]. Seven studies were with a retrospective (12.1%) study design and of the total 13 (22.4%) studies deals with women with bad obstetric history (BOH). These studies detected the presence of maternal anti-rubella IgG as a marker of past infection or immunization and mothers who did not possess these antibodies were susceptible to Rubella infection. Maternal IgM was detected in some studies as a marker of recent or current infection, which is associated with an increased risk of vertical transmission. The range of maternal susceptibility to Rubella was 2.1% to 43% in pregnant women [186,189] and 21.1% – 71.04% in women with BOH [91,190]. Higher susceptibility rates were reported [1,91,93,178,209,210] in Nigeria (84.8%), India (71%), Nepal (50%), Brazil (28.4%), Iran (25%), and Sri Lanka (24%). The higher susceptibility rates for Arab countries excluding Iraq were reported [35,216,220,221] in Morocco (83.4%), Sudan (34.7%), Qatar (25.1%), and Tunisia (20.3%). The lowest susceptibility was reported [217] for Saudi Arabia (6.7%). In Iraq, reports indicate a high susceptibility rates in Thi Qar (98.05%), Kirkuk (91%), Baghdad (79%), and Waset (45.7%). While the lowest susceptibility rates were reported for Diyala (0%) in women with previous abortion, and 3.9% in pregnant women without history of BOH [215]. The same figures was reported later by another research group in Babylon [213].
Article |
Location, setting of study |
Type, duration of study |
Population |
Results |
Lin et al, [166] |
Taiwan, Hospital |
Cross-sectional, 7 yrs |
10,089 pregnant women |
Seronegativity was 14% |
Tamer et al, [167] |
Turkey, Antenatal clinic |
Cross-sectional, |
1972 pregnant women |
Anti-rubella IgG 96.1%
Anti-rubella IgM 0.2% |
Ai & Ee, [168] |
Malaysia, Antenatal & hospital |
Cross-sectional |
500 pregnant women |
Seronegativity 11.4% |
Majlessi et al, [169] |
Iran, PHC |
Cross-sectional, 2 yrs |
965 Pregnant women |
Seronegativity 8.9% |
Das et al, [170] |
India, hospital |
Case control |
1115 pregnant BOH |
Seropositivity 3.6% |
Ocak et al, [171] |
Turkey, Antenatal |
Retrospective, 23 months |
1652 Pregnant women |
Anti-rubella IgG 95%
Anti-rubella IgM 0.54% |
Pehlivan et al, [172] |
Turkey, Community based |
Turkey, Community based |
824 Women |
Anti-rubella IgG 93.8%
Anti-rubella IgM 0.6%
Negative 5.6% |
Tseng et al, [173] |
Taiwan, Hospital |
Retrospective
observational, 4 yrs |
5007 pregnant women |
13.4% susceptible |
Bareto et al, [174] |
Mozambique, antenatal |
Cross-sectional, 3 months |
974 pregnant women |
Anti-rubella IgG 95.3% |
Corcoran & Hardie, [175] |
South Africa, Antenatal clinic |
Cross-sectional |
1200 serum sample |
96.5% immune |
Desinor et al, [176] |
Haiti, hospital |
Cross-sectional, 4 months |
495 pregnant women |
95.2% seropositive |
Weerasekera et al,[177] |
Sri Lanka, antenatal |
Cross-sectional, 2 yrs |
500 pregnant women |
82% positive for rubella IgG |
Palihawadana et al, [178] |
Sri Lanka, antenatal |
Cross-sectional, |
620 pregnant women |
76% seropositive |
Ashrafunnessa Khatun, et
al [179] |
Bangladesh, hospital |
Cross-sectional, 11 months |
609 pregnant women |
14.1% seronegative |
Dos Santos et al, [180] |
Brazil, antenatal |
Cross-sectional, 8 months |
1024 pregnant women |
77.4% seropositive |
Surpam et al [181] |
India, Antenatal clinic |
Case control, |
150 BOH |
4.66% IgM |
Uyar Y et al [182] |
Turkey, Hospital |
Cross sectional, 1 year |
600 Pregnant women |
94.3% IgG, 1.7% IgM |
Karabulut A et al [89] |
Turkey, Antenatal clinic |
Cross sectional, 1 year |
1268 Pregnant women |
95.1% IgG, 0% IgM |
Kumari N et al [1] |
Nepal, Hospital |
Case control, 4 months |
12 BOH |
50% Seropositive |
Nabi SN et al [90] |
Bangladesh, Hospital |
Cross sectional, 10 months |
111 Pregnant women |
81.08% IgG, 6.3% IgM |
Sadik MS et al [91] |
India, Hospital |
Case control, 2 years |
86 BOH |
29.06% IgG, 4.65% IgM |
Fomda BA [183] |
Kashmire, Hospital |
Case control, |
892 Pregnant with
BOH1028 Pregnant with
previous normal pregnancy |
26.12% IgM8.96% IgM |
Bamgboye AE et al [184] |
Nigeria, Antenatal clinic |
Cross sectional, |
159 Pregnant women |
68.5% IgG |
Linguissi LS et al [94] |
Burkina Faso, |
Cross sectional, 3 years |
Pregnant women |
77% IgG |
Jubaida N, et al [185] |
Bangladesh, Outpatient clinic |
Cross sections, 6 months |
134 Pregnant women |
84.33% IgG, 0.75% IgM |
Amina MD et al [186] |
Nigeria, Antenatal clinic |
Cross sectional, 10 months |
430 Pregnant women |
97.9% IgG |
Chopra S et al [36] |
India, Antenatal clinic |
Case control, 1 year |
200 BOH |
17.5% IgM |
Ogbounnaya EC [187] |
Nigeria, Hospital |
Cross sectional, 1 year |
190 Pregnant women |
6.84% IgM |
Koksaldi-Motor et al [95] |
Turkey, Hospital |
Cross sectional, 1 year |
1103 women childbearing
age |
93.6% IgG |
Langiano E et al [188] |
Italy, Hospital |
Cross sectional, 23 months |
1242 Child bearing age |
77.9% IgG |
Onakewhor & Chiwuzie
[189] |
Nigeria, Hospital |
Cross sectional, |
270 Pregnant women |
57% IgG, 91.3% IgM |
Raveendran V et al [190] |
India, Hospital |
Case control, 1 year |
182 BOH |
78.9% IgG, 31.58% IgM |
Fokunang et al [191] |
Cameroon, Hospital |
Cross sectional, 4 months |
211 Pregnant women |
88.6% IgG |
Calimeri S et al [192] |
Italy, Hospital |
Cross sectional, 18 months |
500 Pregnant women |
85.8% IgG |
Corcoran & Hardie [193] |
South Africa, Hospital |
Cross sectional, 1 year |
1200 Pregnant women |
95.3% – 98 % IgG |
Mora- Garcia GJ et al
[194] |
Colombia, Hospital |
Cross sectional, 1 year |
1528 female 10-49 yrs |
93% IgG |
Uysal A et al [195] |
Turkey, Hospital |
Cross sectional, 8 years |
5959 Pregnant women |
97.8% IgG, 0.37% IgM |
Combich JJ et al [196] |
Kenya, Hospital |
Cross sectional, 7 months |
470 Pregnant women |
92.9% IgG |
Kearns MJ et al [197] |
Canada, Provincial Public
Health Laboratory |
Retrospective Observational
study, 3.5 years |
140 473 Pregnant women |
91.2% IgG |
Jahromi AS et al [198] |
Iran, Hospital |
Case control, 8 months |
220 Aborted women |
91.2% IgG, 10.8% IgM |
Ramana BV et al [199] |
India, Hospital |
Case control, |
150 BOH |
12.67% IgM |
Cheong & Khoo [200] |
Malaysia, Hospital |
Cross sectional, |
500 Pregnant women |
11.4% susceptibility |
Honarvar B, et al [201] |
Iran, Hospital |
Cross sectional, 3 months |
138 Pregnant women |
96% IgG |
Nwanegbo et al [202] |
USA, Prenatal care clinic |
Retrospective Cross sectional,
1 year |
642 Pregnant women |
6.9% Non rubella immune |
Eslamian L [203] |
Iran, Hospital |
Cross sectional, 10 months |
500 Pregnant women |
76% IgG |
Ozdemir M et al [204] |
Turkey, Hospital |
Cross sectional, 6 months |
249 Pregnant women |
95.9% IgG, 0.4% IgM |
Adesina OA [205] |
Nigeria, Hospital |
Cross sectional, |
230 Childbearing age
women |
93.5% IgG |
Frischknecht F et al [92] |
Switzerland, Hospital |
Cross sectional, 1 yr |
723 Pregnant women in
labor |
93.08% seropositive |
Ang LW et al [206] |
Singapore, |
Retrospective |
Epidemiological data 1991-
2007 |
84.2% Immune to rubella |
Upreti SR et al [207] |
Nepal, |
Retrospective 2004-2009 |
2224 Childbearing age |
90.8% IgG |
Odland JO, et al [208]
|
Russia, Hospital
|
Case control, 4 months
|
182 Pregnant & 127 Aborted
women
|
77.5% versus 59.8%
seroprevalence
|
Goncalves MA, et al, [97]
|
Brazil, Hospital
|
Retrospective, 2 years
|
574 Pregnant women
|
93.1% IgG, 0.6% IgM
|
Turbadkar D, et al [3]
|
India, Antenatal clinic
|
Case control, 1 year
|
380 BOH
|
61.3% IgG, 26.8% IgM
|
Inagaki ADM, et al [93]
|
Brazil, Antenatal clinic
|
Cross sectional, 1 year
|
9559 Pregnant women
|
71.6% IgG, 0.1% IgM
|
Agbede OO, et al [209]
|
Nigeria, Antenatal clinic
|
Cross sectional, 3 months
|
92 Pregnant women
|
15.2% IgG, 3.3% IgM
|
Ebadi p, et al [210]
|
Iran, Hospital
|
Case control, 3 years
|
120 Aborted women
|
75% seropositive
|
Malarvizhi et al [211]
|
India, Private hospital
|
Cross sectional, 2 years
|
232 Pregnant women
|
50.9% IgG, 3.4% IgM
|
Vilibik-Cavlek T, et al
[96]
|
Croatia, Hospital
|
Cross sectional, 5 years
|
Pregnant & non pregnant
women
|
94.6% IgG, 0% IgM
|
Ballal M et al [165]
|
India, Hospital
|
Case control,
|
334 BOH
|
4.49% IgM
|
Table III. Characteristics and results of studies reporting prevalence of maternal rubella infection.
Article
|
Location, setting of study
|
Type, duration of study
|
Population
|
Results
|
Abdulmohaymen N [99]
|
Iraq (Baghdad), Hospital
|
Case control, 9 months
|
119 Aborted women
|
4.8% IgM recurrent
spontaneous abortion
2.9% IgM non recurrent
spontaneous abortion.
6.5% IgG recurrent
spontaneous abortion
20.6% IgG non recurrent
spontaneous abortion
|
Jasim et al [100]
|
Iraq, Waset, Hospital
|
Case control, 1 year
|
162 Women with
spontaneous abortion
|
54.3% IgG, 62.3% IgM
|
Al- Taie et al [101]
|
Iraq, Mosul, Private laboratory
|
Case control, 1 year
|
100 BOH
|
16% IgM
|
Hadi NJ [130]
|
Iraq, Thi Qar, Hospital
|
Case control
|
190 Aborted women
|
1.05% IgG, 4.21% IgM
|
Salman YG [131]
|
Iraq, Kirkuk, Hospital
|
Case control, 11 months
|
75 BOH
|
8.88% Seropositive,
6.75% IgM
|
Abdul-kareem ET, et al [212]
|
Iraq, Baghdad, Hospital
|
Case control, 8 months
|
79 Aborted women
|
34.2% seropositive
|
Al-rubaii B, et al [214]
|
Iraq, Babylon, Hospital
|
Cross sectional , 14
months
|
250 Childbearing age
women
|
78.33% Pregnant,
75.71% non- pregnant
|
Hasan ARS, et al [215]
|
Iraq, Diyala, PHC
|
Case control
|
46 Pregnant – BOH, 52
Pregnant – Non BOH
47 Non pregnant Without
Abortion
39 Non pregnant with
Abortion
|
IgG- 76%
IgG- 96.1
IgG – 85.1%
IgG- 100%
|
Hammod AM, et al [213]
|
Iraq, Babylon, Hospital
|
Case control, 20.5 m0nths
|
46 Pregnant – BOH,
52 Pregnant – Non BOH
47 Non pregnant Without
Abortion
39 Non pregnant with
Abortion
|
IgG- 76%
IgG- 96.1
IgG – 85.1%
IgG- 100%
|
Hamdan HZ, et al [216]
|
Sudan, Hospital
|
Cross sectional, 2 months
|
231 Pregnant women
|
65.3% IgG, 3.4% IgM
|
Ghazi HO, et al [217]
|
Saudi Arabia, Hospital
|
Cross sectional
|
926 Pregnant women
|
93.3% IgG
|
Al-Marzoqi AHM, et al [129]
|
Iraq, Babylon, Hospital
|
Cross sectional, 6 months
|
180 Pregnant women
|
73.9% IgG,
53.9% IgM
|
Gashout A, et al [140]
|
Libya, Hospital
|
Case control, 5 years
|
692 Aborted women
|
89% IgG, 4.3% IgM
|
Abu- Madi MA, et al [35]
|
Qatar, Hospital
|
Cross sectional, 3 years
|
847 Women > 20 yr age
|
74.9% IgG
|
Barah & Chehada [219]
|
Syria, University Laboratory
|
Cross sectional, 3 months
|
90 university female
students
|
85.6% IgG
|
Caidi H, et al [220]
|
Morocco, Hospital
|
Cross sectional, 1 year
|
967 childbearing age
women 15-39 yrs
|
16.6% IgG
|
Hannachi N, et al [221]
|
Tunisia, Hospital
|
Cross sectional,
|
404 Pregnant women
|
79.7% seroprevalence
|
Al- Hindi A, et al [150]
|
Palestine, IVF centre
|
Retrospective, 6 years
|
1954 Women with infertility
or abortion
|
7% IgM
|
Nama J et al [218]
|
Iraq, Najaf, Hospital
|
Case control, 10 months
|
300 Aborted women
|
77% IgG, 4.66% IgM
|
Table IV. Characteristics and results of studies in Arab countries reporting prevalence of maternal rubella infection.
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