American Journal of Dermatology and Venereology

2013;  2(3): 31-38

doi:10.5923/j.ajdv.20130203.04

Seroprevalence of Herpes Simplex Virus Type 2 (HSV 2) in Women with Bad Obstetric History

Zainab Khalil Mohamed Aljumaili1, Abdulghani Mohamed Alsamarai2, Wesam Suhail Najem3

1Department of Microbiology, Tikrit University College of Medicine, Kirkuk Health Authority, Tikrit, Iraq

2Departments of Medicine and Microbiology, Tikrit University College of Medicine, Asthma, Allergy Centre, Tikrit Teaching Hospital, Tikrit, Iraq

3Department of Dermatology, Tikrit University College of Medicine, Tikrit, Iraq

Correspondence to: Abdulghani Mohamed Alsamarai, Departments of Medicine and Microbiology, Tikrit University College of Medicine, Asthma, Allergy Centre, Tikrit Teaching Hospital, Tikrit, Iraq.

Email:

Copyright © 2012 Scientific & Academic Publishing. All Rights Reserved.

Abstract

HSV 2 is common human pathogen that lead to lifelong latent infection and may be associate with transmission from mother to their fetus. The risk factors associated with HSV 2 seropositivity in pregnant women in Iraq are not known. The present study conducted to verify the prevalence of HSV 2 infections in women with bad obstetric history (BOH) in Kirkuk Governorate. HSV 2 seropositivity among women aged 17 to 47 years was investigated by determination of HSV 2 IgG and IgM in prospective a case control descriptive study. The overall HSV 2 seroprevalence was 24.2%, with a significant difference between women with BOH and women with normal pregnancy. HSV 2 IgM, as an indicator of current infection was demonstrated in 3.2% of the studied population, and was significantly higher in women with BOH compared to women with normal pregnancy. Both HSV 2 IgG and IgM were significantly varied with age groups, with trends of increasing with older ages. HSV 2 IgG was statistically significantly higher in working women as compared to housewife. Significant association was found between HSV 2 seroprevalence and family size and education levels.

Keywords: TORCH, HSV, BOH, IgM, IgG, Kirkuk, Iraq

Cite this paper: Zainab Khalil Mohamed Aljumaili, Abdulghani Mohamed Alsamarai, Wesam Suhail Najem, Seroprevalence of Herpes Simplex Virus Type 2 (HSV 2) in Women with Bad Obstetric History, American Journal of Dermatology and Venereology, Vol. 2 No. 3, 2013, pp. 31-38. doi: 10.5923/j.ajdv.20130203.04.

Article Outline

1. Introduction
2. Patients and Methods
    2.1. Settings
    2.2. Study Design
    2.3. Study Area
    2.4. Study Population
    2.6. Collection of Data
    2.7. Sample Collection
    2.8. Ethical Approval
    2.9. Methods
    2.10. Analysis of Data
3. Results
4. Discussion
5. Conclusions

1. Introduction

Perinatal infections account for 2% to 3% of all congenital anomalies. TORCH, which includes Toxoplasmosis, Other(syphilis, varicella-zoster, parvovirus B19, Human Immunodeficiency Virus and Hepatitis B virus), Rubella, Cytomegalovirus, and Herpes infections, are of the most common infections associated with unfavorable outcome of pregnancy[1].
Herpes genitalis is one of the most common sexually transmitted diseases[2]. Herpes simplex virus type 2 (HSV-2) is the major cause of genital herpes[3]. The incidence of herpes simplex virus (HSV) infection has been increasing steadily in recent decades, and concerns about perinatal HSV infection are growing among women of reproductive age because of the risk of transmission of the virus to their babies during pregnancy, with potentially devastating consequences to the fetus[4].
Little is known about the seroprevalence of HSV 2 in Iraqi women with bad obstetric history[5-7]. These three studies reported a wide range of HSV 2 seropositivity (range from 8.1% to 73.9 for IgM), while other study for Iraq, reported seroprevalence of 28.9% HSV 2 IgM in pregnant women[8]. In addition, the study population of these 3 studies ranged from 100 to 162 subjects, which is lower that sample size required for HSV 2 seroprevalence study. Furthermore, the studies performed in Arab countries reported a range of 0.5%[9] to 7.6%[10] for HSV2 IgM and 6.5%[9] to 27.1% [11] for HSV2 IgG in pregnant women.
The literature review[12] highlights a gap in existing knowledge on the epidemiology and impact of maternal infection, especially on the aetiology of infectious agents that lead to puerperal sepsis and subsequent mortality. Increased surveillance and diagnostic capabilities in healthcare facilities and in the community is needed to identify the aetiological agents responsible for puerperal sepsis and maternal mortality. The prevalence of maternal infection reported by the studies identified in literature regarding HSV 2 may be an underestimate of actual rates of infection as not all pregnant women in Iraq may have access to or choose to access formalized antenatal care. This could be due to financial constraints, difficulties in accessing these facilities and personal or cultural beliefs. In addition, antenatal care services may not have the capacity to routinely screen for maternal infections, especially those that are asymptomatic and those that require serological tests such as PCR and ELISA to diagnose, due to limited resources or expertise. These infrastructural problems are essential contributors to the persistence of high maternal morbidity and mortality in developing countries and need to be overcome in order to accurately characterize the burden of maternal infections in these countries, including Iraq[12].
This literature review highlights the high bacterial and viral maternal infection rates in the developing world. Urgent, concerted action is required to reduce the burden of these infections. In addition to raising awareness about the severity of the problem of maternal infections in Iraq , data from seroepidemiological research will be beneficial in guiding public health policy, research interests and donor funding towards achieving improvement in health care delivery[12]
The aim of this study was to identify seroprevalence of HSV 2 IgG and IgM in women with bad obstetric history compared to those with normal pregnancy and the association of these markers with socio-demographic variables of Iraqi population in Kirkuk Governorate.

2. Patients and Methods

2.1. Settings

Kirkuk General Hospital, Primary Health Care Centers in Kirkuk Governorate.

2.2. Study Design

The study design is a Descriptive Case Control Study.

2.3. Study Area

This descriptive case-control study was conducted at the antenatal clinic of Kirkuk General Hospital and Primary Health Care Centre in Tessean. Women (Pregnant or Non pregnant) with bad obstetric history was recruited from those attending outpatient Gynaecology Clinic Kirkuk General Hospital or the outpatient Clinic at Tessean PHC.

2.4. Study Population

The study population is women with childbearing age. Study population was recruited from Primary Health care Centers located in urban and rural areas in Kirkuk Governorates. In addition, one of the study population group was recruited from pregnant women who were in labor to select the group of pregnant with risky outcomes.
Group 1: Pregnant women with age range of 15-48 years, and with normal pregnancy.
Group 2: Non pregnant women with age range of 15-48 years, and with normal pregnancy.
Group 3: Pregnant women with Risk factor (BOH) depending on their previous pregnancy and /or delivery outcome which include pregnancy loss, intrauterine deaths, preterm deliveries and intrauterine growth retardation. Their age range from 15-48 years.
Group 4: Non- pregnant women with Risk factor depending on their previous pregnancy and /or delivery outcome which include pregnancy loss, intrauterine deaths, preterm deliveries and intrauterine growth retardation. Their age range from 15-48 years.
The demographic information of these groups are shown in Table 1. The target number recruited for each group was 150 women. However, the total number of women included in the study was 538, of them 293 (54.5%) were with BOH, and 245 (45.5%) were with normal pregnancy history. In the BOH group, 144 (49.1%) women were pregnant, while in the normal pregnancy group, 117 (47.7%) were pregnant.
Table 1. Study population
     

2.6. Collection of Data

The designated investigators visited the outpatient department daily, selected the study subjects, and screened them using a predesigned pretested schedule considering the inclusion and exclusion criteria till the study subjects recruitment could be identified. The next available age-matched multiparous antenatal woman without BOH was included in the control group subjects.
Clinical examination and laboratory investigations were carried out for the study subjects to exclude other causes of foetal wastage, such as hypertension, diabetes mellitus, syphilis, Rh (rhesus) incompatibility, physical causes of abortion, and consanguinity. Subjects with known causes of foetal wastage were excluded from the study. All of them were interviewed to ascertain age, medical and obstetric information.

2.7. Sample Collection

For serological analysis, 5-10 mL of venous blood was collected in a sterile container with strict aseptic precautions from each study subject. The serum was separated and stored in numbered aliquots at -20℃ till assayed. All the serum samples collected from the study and control groups were tested for HSV 2 IgM and IgG antibodies by commercially- available (ELISA) kits. The results read by a Microwell reader and compared in a parallel manner with controls; optical density read at 450 nm on an ELISA reader.

2.8. Ethical Approval

The ethical committee of the concerned institute approved the research protocol. The purpose and procedures of the study are to be explained to all the study subjects, and informed consent is to be obtained from them. The study design was approved by the ethical committee of TUCOM that was now registered in USA[U.S. Department of Health and Human Services (HHS) & Registration of an Institutional Review Board (IRB)]. IORG #: IORG0006885.
Institution: Tikrit University College of Medicine [TUCOM] OMB No. 0990-0279

2.9. Methods

ELISA was used for determination of IgM and IgG for HSV-2 and the test was performed according to manufacturer instructions. The kit purchased from BioCheck, Inc, 323 Vintage Park Dr, Foster City, CA 94404.

2.10. Analysis of Data

Collected data were compiled in Microsoft Excel spreadsheet. The proportion and the mean value were computed in appropriate situations. To find out any association between categorical data, Chi square test was employed using the SPSS (Version 16). If the sample size in BOH group not reach the targeted number Power Analysis were performed to determine the accuracy of findings.
The study finding data were presented as frequency ± SD and 95% Confidence Interval. Bivariate Regression Line Analysis to calculate Odd Ratio for determination of association between two variables. The determinants for HSV 2 infection is determined by calculation of Odd Ratio using Logistic Regression Line Analysis. Confounding factors such as age, socio-economic status, e.t.c are standardized when serological determinants were calculated.

3. Results

A total of 600 women were recruited to study, as our target number is 150 women in each group. However, 62 women were defaulted from the study, 7 in women with BOH, and 55 in group of women with normal pregnancy. Thus the study population included in the statistical analysis was as shown in Table 1. There was no significant differences in mean of age between the study groups.
The overall HSV 2 seroprevalence in our study population was 24.2%, with a significant (X2 =37.303, P=0.000) difference between women with BOH (34.5%) and women with normal pregnancy (11.8%). However, there was no significant difference between pregnant and non pregnant women in both BOH and normal pregnancy outcome groups. Table 2. HSV 2 IgM, as an indicator of current infection was demonstrated in 3.2% of the studied population, and was significantly (X2=14.67, P=0.000) higher in women with BOH (5.8%) compared to women with normal pregnancy (0%). There was no significant difference in HSV 2 IgG and IgM seroprevalence between pregnant (IgG =21.8%, IgM=3.1%) and non pregnant (IgG= 26.4%, IgM=3.2) women. Table 3.
Both HSV 2 IgG and IgM were significantly varied with age groups, with trends of increasing with older ages (X2=15.1,P=0.002 for IgG; X2=7.97, P=0.04 for IgM). HSV 2 IgG seroprevalence was lower in women with age of less than 20 years (10.8%), subsequently, increased in women with age of 20-29 years (29.4%), with a higher seroprevalence in women with age of 40-48 years. HSV 2 IgM was not detected in women with age of less than 20 years, however, the higher seroprevalence rate (5.5%) was in women with age of 20 – 29 years. Table 4. OR calculation not confirm the association between HSV 2 IgG and IgM seropositivity and women age of less than 30 years. Table 5.
Table 2. Herpes Simplex virus seroprevalence in women with bad obstetric history
     
Table 3. Herpes Simplex virus seroprevalence in pregnant compared to non-pregnant women
     
Table 4. Frequency of TORCH complex agents in regard to age
     
Table 5. Odd ratio of TORCH agents in regards to age of women lower than 30 years
     
The current infection was higher in urban (3.8%) than that in rural (1.4%) areas, but the difference was not statistically significant (Table 6) and OR not confirmed an association (Table 7). The same pattern was demonstrated for HSV 2 IgG seroprevalence.
Table 6. Frequency of HSV 2 IgG and IgM in regard to sociodemographic characteristics
     
Table 7. Association of HSV 2 seropositivity with sociodemographic characteristics using Bivariate analysis
     
HSV 2 IgG was statistically significantly (P=0.04) higher in working women (36.6%) as compared to housewife (23.1%), however, OR not confirmed an association with mother occupation (OR=0.5218, P=0.05). Tables 6 & 7.
Mother education do influence significantly HSV 2 IgG (X2=44.52, P=0.000) and HSV 2 IgM (X2=10.71, P=0.03) seropositivity and OR confirmed a significant association between education levels and IgG (OR=2.18 – 5.57, P=0.004-0.0001) and IgM seropositivity (OR= 5.03, P=0.007). Tables 6 & 7.
Family size significantly influence HSV 2 IgG (X2=11.3, P=0.001) and IgM (X2=37.2,P= 0.000) seroprevalence and such association was confirmed by OR (IgM, OR=13.88, P<0.0001; IgG, OR=5.01,P=0.002). Tables 6 and 7.

4. Discussion

Infection with herpes simplex is one of the most common sexually transmitted infections. Because the infection is common in women of reproductive age it can be contracted and transmitted to the fetus during pregnancy and the newborn. Herpes simplex virus is an important cause of neonatal infection, which can lead to death or long-term disabilities. Rarely in the uterus, it occurs frequently during the transmission delivery[13].
The greatest risk of transmission to the fetus and the newborn occurs in case of an initial maternal infection contracted in the second half of pregnancy. The risk of transmission of maternal-fetal-neonatal herpes simplex can be decreased by performing a treatment with antiviral drugs or resorting to a caesarean section in some specific cases[13].
Some trends may be drawn from a review of type-specific HSV prevalence in different geographic areas and subpopulations[14]. First, HSV-2 prevalence is highly variable and depends on many factors, including country and region of residence, population subgroup, sex, and age. Second, HSV-2 prevalence is, in general, higher among higher risk sexual behavior groups. Third, HSV-2 prevalence is generally higher in women than men. Fourth, HSV-2 prevalence is strongly associated with age, increasing from negligible levels in children younger than 12 years to as high as 80% among higher risk populations. Fifth, in a given population and age group, HSV- 1 prevalence is almost always greater than HSV-2 prevalence. Striking variations in HSV-2 prevalence were noted in different geographic regions. HSV-2 prevalence is highest in areas of Africa and parts of the Americas. In western and southern Europe, HSV-2 prevalence is usually lower than in northern Europe and North America. In Asia, HSV-2 prevalence appears lower than in other geographic areas. Direct comparisons in overall prevalence from independent studies should be made with caution given substantial differences in the populations surveyed, age distributions, and HSV serologic test methods.
Comparisons of age-specific HSV-2 prevalence among similar populations in different regions may be useful and further data acquired by using the same serologic methods would be desirable. HSV-2 prevalence was consistently higher in higher risk populations compared with those considered at a lower risk. In some countries such as the USA, HSV-2 prevalence was strongly dependent on race; black Americans had a much higher prevalence of infection than whites and Mexican Americans of all ages. These results suggest that within populations, the risk of acquiring HSV-2 infection is highly variable[14]
In the present study, an overall HSV IgG seroprevalence of 24.2% was found among women, and it was significantly (X2= 37.303, P=0.000) higher in women with BOH (34.5%) as compared to women with normal pregnancy (11.8%). However, there was no significant difference in seroprevalence between pregnant and non pregnant women, but was higher in non pregnant than pregnant women. This study HSV 2 seroprevalence (11.82%) in pregnant women was about similar to that reported for China,(10.8%)[15], Indonesia (9.9%)[16], Bangladesh (9.91%)[17], and UK (10.4%)[18]. In contrast to our study, a much higher HSV 2 seroprevalence has been reported from Zimbabwe (51.1%)[19], Germany (82%)[20], Turkey (63.1%)[3], and Iran (43.75%)[21]. In addition, our finding was lower than that that reported for Tanzania (20.7%)[22], Australia (30%) [23], USA (22%)[24], Switzerland (21.2%)[25], Canada (17.3%)[26], Senegal (22%)[27], Belgium (18.2%)[28] , China (23.5%)[29], and Korea (17%)[30]. However, the present study seroprevalence was higher to that reported for Turkey (4.4%-5%)[31,32], Kashmir (7.5%)[33], India (8.7%)[34], Croatia (6.8%)[35], Italy (7.6-8.4%)[13].
In women with BOH, our HSV2 IgG seroprevalence (34.5%) was about similar to that reported for India(33.58%) [36] and Nepal (33.3%)[37]. However, it was higher to that reported for India (16.8-18.6%)[38,39]. Furthermore, the seroprevalence was much lower to that reported for Waset (60.6%), Iraq[6] in women with spontaneous abortion. In pregnant women, this study HSV IgG seroprevalence was lower to that reported for Saudi Arabia (27.1%)[11], Qatar (26.3%)[10], Babylon, Iraq (22.2%)[8] and Syria (52%)[40]. However, it was higher to that reported other two studies in Saudi Arabia (6.5-6.8%) [9,41].
The HSV 2 IgG seroepidemiology varies between different countries, and between groups of individuals depending on the demographic and clinical characteristics of the population. For example, studies performed in Iraq (11.1-60.6%), Saudi Arabia (6.5-27.1%), and Turkey (4.4%-63.1%), demonstrated a wide range of seroprevalence. These variations may be attributed to various sexual behavior, number of previous pregnancies, duration of sexual activity, residence, education, occupation and socioeconomic status[33,34,41-44]
Seropositivity in the present study was found to be highly associated with history of previous abortion[X2=37.303, P=0.000), a finding agreed to that reported by others[43,45]. In our study, the HSV 2 IgG seroprevalence rose steadily with age (10.9% among women aged 15-19 to 29.4% among women aged 20-29 years. There was a significant variation (X2=15.1, P=0.002) in HSV 2 IgG seroprevalence between age groups. These findings are comparable to studies reported for other geographical areas[3,23,28,33,41-52].
Residence not seems to influence HSV 2 seroprevalence as this study demonstrated a non significant differences between rural (23.6%) and urban (24.4%) areas. OR not confirmed an association between residence and HSV 2 seroprevalence. This findings agreed to that reported by Rathore et al[33] , however, Chawla et al[48] suggested an association between residence (urban middle class) and HSV 2 seroprevalence.
HSV 2 IgG seroprevalence was significantly (X2=3.73, P=0.04) higher in working women (36.6%) as compared to housewife (23.1%) women, however, OR not confirm such association. These findings agreed to that reported by others[32,33,34,52], while one study from Saudi Arabia[41] reported an association, but when the data grouped as we do, no such significant association was achieved.
HSV 2 IgG seroprevalence was significantly (X2= 44.52, P=0.000) varies according to women education levels in our study and this association was confirmed by OR using bivariate analysis (OR= 2.18 – 5.57, P=0.004-<0.0001). The seroprevalence was steady increased with education, same to that reported by Chawla et al[48] and Xu et al[47], while other studies show high seroprevalence in less educated women[46,41,42]. However, Biswas et al[34] reported higher incidence in women with secondary school education. Page et al[53], showed the highest prevalence of HSV 2 in women with the lowest education level residing in the highest socioeconomic status area. Rathore et al[33] and Agabi et al[52] not found a significant association between HSV seroprevalence and education levels.
In this study, HSV IgG seroprevalence was significantly higher (X2=11.3, P=0.001) in small size families (crowding index) as compared to large size families and this association confirmed by OR calculation (OR=5.0114, P=0.002). HSV infection is increased with the increase in sexual activity and thus small size families may provide comfortable environment that encourage sex performance. In addition, young women receiving family planning services are at risk for herpes simplex virus type 2 (HSV-2) infection[54].
The literature indicated a paradox in association between HSV 2 seropositivity and lower income and this could be due to differences in risk behavior among the different income groups. It was seen in a study performed for India[34], that majority of Muslims subjects (84.9%;90/106) were from low income group. It was also observed that Muslims subjects had the lowest HSV 2 seroprevalence (3.8%) compared to Hindu (5.8%) and Christians (12.6%), which may explain that disparity. The suggested risk factors that lead to high HSV 2 seropositivity in developed and some undeveloped countries are not applicable in our society due to religious and social reasons. Thus other risk factors are to be speculated in our society, one of these is the male circumcision, as it lowers the prevalence of HSV 2[55]. Recently reported study[33], higher HSV 2 seroprevalence was found among Christians versus Muslims and this differences in prevalence with religions, may be due to practice of male circumcision at infancy or early childhood by the spouses of the pregnant women among Muslims.
Low socioeconomic status observed in some studies to be associated with HSV 2 seroprevalence[33,34,44,48,53]. However, Germany as a country with high socioeconomic status, the HSV 2 seroprevalence was 82% in pregnant women, while the corresponding value in Arab countries ranged from 6.5% to 27.1%. Thus Islamic legislation concerning faithful family relations and personal hygiene are an important factors that reduce HSV 2 infection.
HSV 2 IgM seroprevalence was 3.2% indicating that current infection of 3.2% in our study population, and it was significantly higher (X2=14.67, P=0.000) in women with BOH (5.8%) as compared to women with normal pregnancy (0%), and about the same in pregnant and non pregnant women. Our HSV IgM (3.1%) seroprevalence in pregnant women was higher than that reported for Turkey (0%)[31], Saudi Arabia (0.5%)[9], Croatia (1.2%)[35], and Bangladesh (1.8%)[17]. Higher seroprevalence was reported for Babylon, Iraq (28.9%)[8], Turkey (13.8%)[3], and Qatar (7.6%)[10].
In women with BOH, HSV IgM seroprevalence (5.8%) was lower than that reported for India[38,56] , Baghdad, Iraq[5], Waset, Iraq[6], Mosul, Iraq[7] and higher to that reported in two studies in India[36,57]. Thus current infection with HSV 2 was lower to that reported in other Iraqi Governorates.
The present study shows a significant variation in current HSV 2 infection between age groups (X2=7.97, P=0.047), the highest incidence in women with age of 20-29 years (5.5%) old, while the lowest rate in women of <19 years old. Using Bivariate analysis , OR not confirmed an association between HSV 2 current infection and age of <30 or > 30 years old, residence, and occupation. However, current infection of HSV 2 was significantly higher (X2=37.2, P=0.000) in large size families (> 3 crowding index) than small size families. OR confirmed the association between current HSV infection and family size (OR=5.0114, P=0.002).

5. Conclusions

The present study indicated a significant association between HSV 2 IgG and IgM and bad obstetric history. The overall HSV 2 seroprevalence in our study population was 24.2%, with a significant difference between women with BOH and women with normal pregnancy. Significant association was found between HSV 2 seroprevalence and family size and education levels. However, HSV 2 seroprevalence was different due to residence, occupation and age of < 30 years, but OR not demonstrate significant association.

References

[1]  Johnson P, Barnes R, Hart C, Francis W: Determinants of immunological responsiveness in recurrent spontaneous abortion. Transpl; 38(3):280-4, 1994.
[2]  Howard M, Sellors JW, Jang Dl. Regional distribution of antibodies to herpes simplex virus type 1 (HSV-1) and HSV-2 in men and women in Ontario, Canada. J Clin Microbiol ;41: 84-89,2003.
[3]  Duran N, Fugen Y, Cuneyt E, Fatih K. Asymptomatic herpes simplex virus type 2 (HSV-2) infection among pregnant women in Turkey. Indian J Med Res ;120, 106-110,2004..
[4]  Duran N. Serological Evaluation of HSV-1 and HSV-2 Infection In Pregnancy. Turk J Med Sci 37: 97-101,2003.
[5]  Abdul Mohymen N, Hussien A, Hassan FK. Association between TORCH agents and recurrent spontaneous abortion. Iraqi J Med Sci 7:40-46,2009.
[6]  Jasim M, Majeed HA, Ali AI. Performance of Serological Diagnosis of TORCH Agents in Aborted versus non aborted Women of Waset province in Iraq. Tikrit Medical Journal 17(2): 141-147,2011.
[7]  AL – Taie AAD. Serological Study For TORCH Infections In Women With High Delivery Risk Factors In Mosul. Tikrit Journal of Pure Science 15:193-198,2010.
[8]  Al-Marzoqi AHM, Kadhim RA, Aljanabi DKF, Hussein HJ, Al Tae ZM. Seroprevalence study of IgG and IgM Antibodies to Toxoplasma, Rubella, Cytomegalovirus, Chlamydia trachomatis and Herpes simplex II in Pregnancy women in Babylon Province. Journal of Biology, Agriculture and Healthcare 2:159-164,2012..
[9]  Alzahrani1 AJ, Obeid OE, Almulhim AA, Awari B, Taha A, et al. Analysis of Herpes Simplex 1 and 2 IgG and IgM Antibodies in Pregnant Women and their Neonates. Saudi J Obstet Gynaecol 5:53-57,2005.
[10]  Abu-Madi MA, Behnke JM, Dabritz HA: Toxoplasma gondii seropositivity and co-infection with TORCH pathogens in high-risk patients from Qatar. Am J Trop Med Hyg 82;(4.); 626-33,2010.
[11]  Ghazi, HO, Telmesani, AM, Mahomed, MF. Torch agents in pregnant Saudi women. Med. Princ. Pract. 11, 4:180-90, 2002.
[12]  Alsamarai AGM, Ajumaili ZK. Seroepidemiology of Toxoplasma, Rubella, Cytomegalovirus and Herpes Simplex Virus -2 in Women with Bad Obstetric History: A Review. Science International, 2013.
[13]  Straface G, Selmin A, Zanardo V, Santis MD, Ercoli A, Scambia G. Herpes Simplex Virus Infection in Pregnancy. Infectious Diseases in Obstetrics and Gynecology Volume 2012, Article ID 385697, 6 pages doi:10.1155/2012/385697.
[14]  Smith JS, Robinson NJ. Age-specific prevalence of infection with herpes simplex virus types 2 and 1: a global review. Journal of Infectious Diseases 186:S3–28,2002.
[15]  Chen X, Yin Y, Chen L, Yu Y, Wei W, Thuy NTT, et al. Herpes simplex virus 2 infection in women attending an antenatal clinic in Fuzhou, China. Sex Transmit Infect 83:369–370,2007.
[16]  Joesoef MR, Sumampouw H, Linnan M, Schmid S, Idajadi A, Louis ME et al. Sexually transmitted diseases in pregnant women in Surabaya, Indonesia. Am J Obstet Gynecol 174:115–119,1996.
[17]  Nabi SN, Wasey A, Haider KMTS, Khan AA, Hoque MM. Seroprevalen of TORCH antibody in pregnant women. Journal of Armed Forces Medical College 8:35-39,2012.
[18]  Ades AE, Peckham CS, Dale GE, Best JM, Jeansson S. Prevalence of antibodies to herpes simplex virus types 1 and 2 in pregnant women, and estimated rates of infection. J Epidemiol Community Health. 43(1):53-60,1989.
[19]  Kurewa NE, Mapingure MP, Munjoma MW, Chirenje MZ, Rusakaniko S, Stray-Pedersen B. The burden and risk factors of sexually transmitted infections and reproductive tract infections among pregnant women in Zimbabwe. BMC Infect Dis.10:e127,2010.
[20]  Sauerbrei A, Schmitt S, Scheper T, Brandstنdt A, Saschenbrecker S, Motz M, Soutschek E, Wutzler P. Seroprevalence of herpes simplex virus type 1 and type 2 in Thuringia, Germany, 1999 to 2006. Euro Surveill. 16(44): pii=20005, 2011.. Available online:http://www.eurosurveillance.org/ViewArticle.aspx? ArticleId=20005
[21]  Shahraki AD, Moghim S, Akbari P. A survey on herpes simplex type 2 antibody among pregnant women in Isfahan, Iran. J Res Med Sci 15(4): 243,2010.
[22]  Yahya-Malima KI, Evjen-Olsen B, Matee MI, Fylkesnes K, Haarr L. HIV-1, HSV-2 and syphilis among pregnant women in a rural area of Tanzania: prevalence and risk factors. BMC Infect Dis 8:e75,2008.
[23]  Haddow LJ, Sullivan EA, Taylor J, Abel M, Cunningham AL, Tabrizi S. Herpes simplex virus type 2 (HSV-2) infection in women attending an antenatal clinic in the South Pacific island nation of Vanuatu. Sex Transmit Dis. 34:258–261, 2007.
[24]  Xu F, Markowitz LE, Gottlieb SL, Berman SM. Seroprevalence of herpes simplex virus types 1 and 2 in pregnant women in the United States. Am J Obstet Gynecol 196(1):43.e1-6,2007.
[25]  Kucera P, Gerber S, Marques-Vidal P, Meylan PR. Seroepidemiology of herpes simplex virus type 1 and 2 in pregnant women in Switzerland: an obstetric clinic based study. Eur J Obstet Gynecol Reprod Biol. 160(1):13-7,2012.
[26]  Patrick DM, Dawar M, Cook DA, Krajden M, Ng HC, Rekart ML. Antenatal seroprevalence of herpes simplex virus type 2 (HSV-2) in Canadian women: HSV-2 prevalence increases throughout the reproductive years. Sex Transm Dis. 28(7): 424-8,2001.
[27]  Diawara S, Toure Kane C, Legoff J, Gaye AG, Mboup S, Bélec L. Low seroprevalence of herpes simplex virus type 2 among pregnant women in Senegal. Int J STD AIDS. 2008;19(3):159-60,2008..
[28]  Bodeus M, Laffineur K, Kabamba-Mukadi B, et al. Seroepidemiology of herpes simplex type 2 in pregnant women in Belgium. Sex Transm Dis 31:297–300,2004.
[29]  Li JM, Chen YR, Li XT, Xu WC. Screening of Herpes simplex virus 2 infection among pregnant women in southern China. J Dermatol. 38(2):120-4,2011.
[30]  Kim D, Chang HS, Hwang KJ. Herpes Simplex Virus 2 Infection Rate and Necessity of Screening during Pregnancy: A Clinical and Sero-epidemiologic Study. Yonsei Med J 53(2):401-407,2010.
[31]  Ozdemir M, Kalem F, Feyzioglu B, Bysal B. Investigation of viral pathogen during pregnancyin a city region in Turkey. Anatol J Clin Invest 5:78-81,2011.
[32]  Dolar N, Serdaroglu S, Yilmaz G, Ergin S. Seroprevalence of herpes simplex virus type 1 and type 2 in Turkey. J Eur Acad Dermatol Venereol. 20(10):1232-6, 2006..
[33]  Rathore S, Jamwal A, Gupta V. Herpes simplex virus type 2: Seroprevalence in antenatal women. Indian J STD & AIDS 31:11-15,2010.
[34]  Biswas D, Borkakoty B, Mahanta J, Walia K, Saikia L, Akoijam BS. Seroprevalence and risk factors of herpes simplex virus type-2 infection among pregnant women in Northeast India. BMC Infectious Diseases 11:325-333,2011.
[35]  Vilibik-Cavlek T, Ljubin-Sternak S, Ban M, Kolaric B, Sviben M, Mlinaric-Galinovic G. Seroprevalence of TORCH infections in women of childbearing age in Croatia. J Matern Fetal Neonatal Med. 24(2):280-3
[36]  Turbadkar D, Mathur M, Rele M: Seroprevalence of TORCH infection in bad obstetric history. Indian J Med Microbiol 21:108-11, 2003.
[37]  Kumari N, Morris N, Dutta R, Is screening of TORCH worthwhile in women with bad obstetric history: an observation from eastern Nepal. J Health, Pop Nutr 29(1): 77–80,2011.
[38]  Haider M, Rizvi M, Khan N, Malik A. Serological study of herpes virus infection in female patients with bad obstetric history. Biology and Medicine, 3 (2) Special Issue: 284-290, 2011.
[39]  Sadik MS, Fatima H, Jamil K, Patil C. Study of TORCH profile in patients with bad obstetric history. Biology Medicine 4:95-101,2012.
[40]  Barah F. Prevalence of herpes simplex types 1 and 2, varicella zoster virus, cytomegalovirus, immunoglobulin G antibodies among female university students in Syria. Saudi Med J 33:990-994,2012.
[41]  Obeid OE. Prevalence of herpes simplex virus types 1 and 2 and associated sociodemographic variables in pregnant women attending King Fahd Hospital of the university. J Fam Commun Med 14:3-7,2007.
[42]  Tidemam RL, Taylor J, Marks C, Seifert C, Berry G, Trudinger B, et al. Sexual and demographic risk facrors for herpes simplex type 1 and 2 in women attending an antenatal clinic. Sex Transm Infect 77:413-5,2001.
[43]  Breinig MK, Kingsley LA, Armstrong JA, Freemam DJ, Ho M. Epidemiology of genital herpes in Pittsburgh: Serologic, sexual and racial correlates of apparent and inapparent herpes simplex infections. J Infect Dis 162:299-305,1990.
[44]  Jennings JM, Louis TA, Ellen JM, et al. Geographic prevalence and multilevel determination of community level factors associated with herpes simplex virus type 2 infection in Chennai, India. Am J Epidemiol 167:1495-1503,2008.
[45]  Frenkel LM, Garraty EM, Shen JP, Wheeler N, Clark O, Bryson YJ. Clinical reactivation of herpes simplex virus type 2 infection in seropositive pregnant women with no history of genital herpes. Ann Intern Med 118:414-8,1993.
[46]  Fleming DT, McQuillan GM, Johnson RE, Nahmias AJ, Aral SO, Lee FK, et al., Herpes simplex virus type 2 in the Unites States, 1976–1994. New Eng J Med 337: 1105–1111,1997.
[47]  Xu F, Sternberg MR, Gottlieb SL, Berman SM, Markowitz LE, Forhan SE, Taylor LD. Serprevalence of herpes simplex virus type 2 among person aged 14-49 years- United States, 2005-2008. MMWR 59:456-459,2010.
[48]  Chawla R, Bhalla P, Bhalla K, Sing MM, Garg S. Community based study on seroprevalence of herpes simplex type 2 infection in New Dwlhi. Indian J Med Micrbiol 26t:34-39,2008.
[49]  Sierra CA, Bedoya AM, Paris S, Baena A, Gaviria AM, Rojas CA, Arbelaez MP, Sanchez GI. Prevalence of specific herpes simplex virus-2 antibodies and associated factors in women of a rural town of Colombia. Trans R Soc Trop Med Hyg. 105(4):232-8,2011..
[50]  Uribe-Salas F, Palma-Coca O, Sánchez-Alemán MA, Olamendi M, Juárez-Figueroa L, Conde-Glez CJ. Population- based prevalence of antibodies against herpes simplex virus type 2 and socio-demographic characteristics in Mexico. Trans R Soc Trop Med Hyg. 103:151-8,2009.
[51]  Howard M, Sellors JW, Jang J, Robinson NJ, Fearon M, Kaczorowski J, Chernesky M. Regional Distribution of Antibodies to Herpes Simplex Virus Type 1 (HSV-1) and HSV-2 in Men and Women in Ontario, Canada. J Clin Microbiol 41: 84–89,2003.
[52]  Agabi YA, Banwat EB, Mawak JD, Lar PM, Dashe N, Dashen MM, Adoga MP, Agabi FY, Zakari H. Seroprevalence of herpes simplex virus type-2 among patients attending the Sexually Transmitted Infections Clinic in Jos, Nigeria. J Infect Dev Ctries. 4(9):572-5,2010.
[53]  Page A, Taylor R, Richters J, Shaw J, Taylor J, Cunningham A, Mindel A. Upstairs and downstairs : socioeconomic and gender interactions in herpes virus type 2 seroprevalence in Australia. Sex Transm Dis 36:344-9,2009.
[54]  Moss NJ, Harper CC, Ahrens K, Scott S, Kao S, Padian N, Raine T, Klausner JD. Predictors of incident herpes simplex virus type 2 infections in young women at risk for unintended pregnancy in San Francisco BMC Infectious Diseases 2007, 7:113 doi:10.1186/1471-2334-7-113
[55]  Tobian AAR, Serwadda D, Quinn TC, Kigozi G, Gravitt PE, Laeyendecker O, Charvat B, Ssempijja V, Riedesel M, Oliver AE, Nowak RG, Moulton LH, Chen MZ, Reynolds SJ, Wawer MJ, Gray RH: Male circumcision for the prevention of HSV-2 and HPV infections and syphilis. N Engl J Med 360:1298-1309,2009.
[56]  Surpam RB, Kamlakar UP, Khadse RK, Qazi MS, Jalgaonkar SV. Serological study for TORCH infections in women with bad obstetric history. J Gynec Obstet India 56:41-43,2006.
[57]  Gumber S, U Arora, P Devi Occurrence of cytomegalovirus and herpes simplex virus infections in pregnancy. Indian J Med Microbiol 26:204-205,2008.