2013.4-21.SeroepidemiologyI

                                                                                                                            article in PDF  
Our Dermatol Online.  2013; 4(4): 522-535
DOI:.  10.7241/ourd.20134.135
Date of submission:  18.07.2013 / acceptance: 04.10.2013
Conflicts of interest: None
 

SEROEPIDEMIOLOGY OF TOXOPLASMA, RUBELLA, CYTOMEGALOVIRUS AND HERPES SIMPLEX VIRUS -2 IN WOMEN WITH BAD OBSTETRIC HISTORY. PART I: TOXOPLASMA AND RUBELLA INFECTIONS

Abdulghani Mohamed Alsamarai1, Zainab Khalil Mohamed Aljumaili2

1Departments of Medicine, Tikrit University College of Medicine, Tikrit, Iraq
2Departments of Microbiology, Tikrit University College of Medicine, Tikrit, Iraq
 

Corresponding author:  Prof. Abdulghani Mohamed Alsamarai    e-mail: galsamarrai@yahoo.com


 

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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