Seroprevalence and Risk Factors of Sexually Transmitted Blood-Borne Infections among Pregnant Women Attending Antenatal Care in Jirapa, Upper West Region of Ghana

Background Sexually transmitted blood-borne infections (STBBIs) contribute to negative outcomes of pregnancy. Hepatitis B virus (HBV), hepatitis C virus (HCV), human immunodeficiency virus (HIV), and syphilis infections in pregnancy contribute significantly to maternal and child morbidities and mortalities. This study assessed the prevalence, knowledge, and risk factors of STBBIs (HBV, HCV, HIV, and syphilis) among pregnant women attending antenatal clinics in Jirapa. Methods A cross-sectional study design involving 246 pregnant women was employed for the study. A structured questionnaire was used to solicit information about the knowledge, prevalence, and risk factors of STBBIs. Results The overall prevalence of STBBIs was 11.4%; HBV prevalence was 9.8% and 0.8% each for HCV, HIV, and syphilis. About 66% of mothers were aware of mother-to-child transmission of infections during pregnancy. Knowledge of transmission of HIV (93.9%), hepatitis (67.1%), and syphilis (53.7%) in pregnancy was relatively high. Knowledge of risk factors for HIV, hepatitis, and syphilis was 97.6%, 74.4%, and 76.0%, respectively. More than 98% of respondents knew about the prevention of HIV, hepatitis, and syphilis. Significant risk factors associated with and predictive of STBBIs were female genital mutilation (FGM) and gravidity. Conclusion The occurrence of STBBIs among pregnant women was strongly associated with FGM and gravidity. Public health education should be directed at stopping the practice of FGM and improving reproductive health in the study area.


Introduction
Pregnancy is usually accompanied by immunologic changes which induce a state of predisposition and susceptibility to various forms of infections [1] and could increase maternal anxiety and uncertainty about pregnancy outcomes [2].
Sexually transmitted blood-borne infections (STBBIs), including human immunodefciency virus (HIV), syphilis, hepatitis B virus (HBV), and hepatitis C virus (HCV), are infections transmitted during sexual contact via blood and or other body fuids. In developing countries, infectious disease prevalence is relatively high, and STBBIs are particularly important in determining the outcome of pregnancies [3].
In 2016, the World Health Organization (WHO) approximated 376 million new sexually transmitted infections with one of four of the following infections: trichomoniasis (156 million), chlamydia (127 million), gonorrhea (87 million), and syphilis (6.3 million). Currently, sexually transmitted infections acquired daily are estimated at more than 1 million. Also, approximately 240 million people globally are living with chronic hepatitis B although hepatitis B infection is vaccine-preventable [4].
Sexually transmitted and blood-borne infection prevention and control have widespread public health benefts and contribute to progress toward the sustainable development goals. To reduce pregnancy-related complications and improve pregnancy outcomes, the WHO recommended Focused Antenatal Care, which includes routine screening for STBBIs during antenatal visits [5,6]. Complications resulting from STBBIs are among the major causes of maternal and neonatal morbidity and mortality during pregnancy [7].
Many women and adolescents lack knowledge about STBBIs and relevant services, including prevention and management [8].
STBBIs in pregnancy are particularly associated with detrimental afterefects to both the baby and the mother [5] and may lead to spontaneous abortion, preterm birth, fetal infection, and psychosocial stress on the mother [9].
In this study, authors assessed the knowledge and prevalence of STBBIs (syphilis, HBV, HCV, and HIV) and associated risk factors in pregnancy.

Study Setting and Subjects.
Tis cross-sectional study targeted pregnant women attending antenatal clinic at the St. Joseph Hospital in the Jirapa municipality. Te hospital is the only referral hospital in the Jirapa municipality, located in Jirapa in the upper west region, Ghana. Te hospital has the following units through which it provides services to patients: pediatric, surgical, medical, obstetric, physiotherapy, outpatients' department and diagnostic (radiology and laboratory services). Te antenatal services are provided by the obstetric unit of the hospital.

Sample Size Estimation.
Te sample size was estimated using Yamane's formula [10]: where n � the desired sample size, N � the population size estimated at 590 from the antenatal attendance records, and e � acceptable sample size error assumed at 5% (level of precision) at a confdence level of 95%. Tis gave a minimum sample size of 238 participants for the study. However, a sample of 246 was achieved.

Data Collection.
A structured questionnaire was designed with some modifcations [11] and used to obtain information from respondents from August to November 2019. Te data obtained included respondents' sociodemographic characteristics, obstetric characteristics, knowledge, and risk factors of STBBIs in pregnancy. Te respondents' status of HBV, HCV, HIV, and syphilis was obtained from the laboratory analysis of 5 mls of blood obtained from each participating pregnant woman into an EDTA tube. Tese tests are part of the Ghana Health Service's mandatory screening protocols for antenatal attendees. Rapid diagnostic test cassettes (Innovita Biological Technology Co. Ltd., China) were used for the screening for hepatitis B surface antigen (HBsAg), anti-HCV, and syphilis according to manufacturer protocols. HIV screening was according to the national rapid testing algorithm using HIV frst response test kit and Ora quick (MoH, Ghana). All positive tests for HIV were confrmed using ELISA.

Data Analysis.
Te data were entered in Microsoft Excel version 2016. Tis was later exported to the Statistical Package for Social Sciences (SPSS) version 25 for analysis. Categorical variables were presented as proportions. Continuous variables were presented as means with standard deviation. Te knowledge score was calculated from 13 structured questions on STBBIs in pregnancy, preventive practices, signs and symptoms, and transmission. A correct answer was awarded 1 point. An overall score below the 50 th percentile was classifed as poor, between the 50 th and the 75 th percentile as moderate, and above the 75 th percentile as good knowledge. Te continuous variables, gravidity, and parity were classifed. Gravidity (number of pregnancies) was classifed into two groups: primigravida (1 pregnancy), and multigravida (2 or more pregnancies). Also, parity (number of births) was classifed into three groups: nullipara (no birth), primipara (1 birth), and multipara (2 or more births).
Te chi-square test was used to compare proportions. To determine the associated risk factors of STBBIs in pregnancy, we performed univariate logistic regression analysis. A risk factor was signifcant at p < 0.05. All variables that met the assumptions for analysis in univariate analysis were further analyzed in a multiple logistic model. For the purpose of the analysis, the presence of STBBIs was calculated as being positive for either HBV, HCV, HIV, or syphilis. Other categorical responses to some risk factors were categorized as "Yes" or "No" and include a family history of HBV, HCV, and HIV infection. Education was reclassifed as low (having at most primary education) and high (having at least high school education). Te profession was categorized as "Salaried" and "Nonsalaried," and "Age" as ≤mean (26) and >mean (26).

Ethical Statement.
Te study was approved by the ethics review board of Tamale Teaching Hospital (TTH/R&D/SR/ 151) and followed the ethical guidelines of St Joseph's Hospital. Te aim and purpose of the study were explained to all respondents. A written informed consent was obtained from respondents to participate in the study.

Respondents' Sociodemographic Characteristics.
A total of 246 respondents were included in the study. Teir ages ranged from 13.0 to 45.0 years with a mean age of 26.3 ± 6.2 years. Christianity constituted the dominant religion of the respondents (87.8%) while 85.4% of the respondents were married. Te literacy rate was 79.9% with the educated having a variable level of education: tertiary (16.7%), secondary (17.0%), and primary (47.2%). Despite this, only 16.3% of the respondents were engaged in formal employment as shown in Table 1.
Among the respondents, 57.2% had body scarifcations while 23.2% of them had female genital mutilation (FGM). History of blood transfusion, abortion, and other STBBIs were recorded in 10.2%, 13.8%, and 6.1% of the respondents, respectively. Overall, 13.8% of the respondents confrmed they have been vaccinated against HBV (Table 1).
With respect to the obstetrics history, the gravidity of the respondents ranged from 1 to 8 pregnancies with a mean gravidity of 2.4 ± 1.5 pregnancies. While 36.6% of the respondents were primigravidae, 63.4% were multigravida with 8.9% being grand multigravida. Te parity of the respondents ranged from 0 to 7 live births with a mean parity of 1.2 ± 1.4. In all, 39.9% were nulliparous, 26.8% were primiparous, and 33.8% were multiparous with 4.1% being grand multiparous (Table 1).

Respondents' Knowledge of Sexually Transmitted Diseases and Risk Factors.
In all, greater than half (50%) of the pregnant women knew the clinical signs and presentation, prevention, transmission, and risk factors of HBV, HCV, HIV/AIDS, and syphilis as shown in Table 2. Te overall knowledge level of the respondents was scored from 7 to 13. Te mean score was 11.0 ± 1.7. Based on the knowledge level classifcation, the knowledge rating was good in 81.7% (201) of the respondents and moderate in 18.3% (45), and none had a poor knowledge level.

Prevalence of Sexually Transmitted Blood-Borne Infections among
Participants. In all, 11.4% of the respondents were infected with one or more of the STBBIs investigated. Specifcally, the prevalence of the studied infections was 9.8% for HBV and 0.8% each for HCV, HIV, and syphilis as shown in Figure 1. HBV coinfection with syphilis 1(0.4%) and with HCV 1(0.4%) was observed (data not shown).

Sexually Transmitted Blood-Borne Infections Associated
Risk and Predictive Factors. Univariate logistic regression analysis revealed female genital mutilation (FGM) and gravidity were signifcantly associated with the occurrence of STBBIs studied. Knowledge of STBBIs was not associated with the occurrence of STBBIs (Table 3). In the multiple logistic regression analysis, FGM (OR � 2.88, 95% CI � 1.3-6.5, p � 0.01) and gravidity (OR � 2.19, 95% CI � 1.1-7.9, p � 0.04) signifcantly infuenced the occurrence of STBBIs. Te odds of a pregnant woman with FGM with STBBIs increased by 1.88 times compared with a pregnant woman without FGM. Also, the odds of a multigravida compared with a primigravida pregnant woman with STBBIs increased by 1.19 times as shown in Table 3.
We further stratifed the various STBBIs studied to investigate their infuencing factors among pregnant women. Only HBV infection met the criteria for analysis as shown in Table 4. Univariate analysis revealed FGM and family history of HBV infection were signifcantly associated with HBV infection among pregnant women (p < 0.05). Further analysis using multiple logistic regression revealed FGM (OR � 3.08, 95% CI � 1.1-8.7, p � 0.03) signifcantly infuencing the occurrence of HBV infection. Te presence of FGM increased the odds of HBV infection by 2.08 times compared with a woman without FGM as shown in Table 4.

Discussion
STBBIs are a public health burden and disproportionately afect women globally. Intrapregnancy STBBIs are particularly associated with adverse pregnancy outcomes [5]. However, antenatal screening services and treatment for infections such as syphilis and HIV have been proven effective in pregnancy outcomes [12,13]. Terefore, antenatal screening services for STBBIs, integrated with the provision of syndromic management of infections during pregnancy in antenatal clinics, should be prioritized. Te prevalence of the STBBIs among pregnant women in Jirapa municipality was 11.4%, higher than other prevalence studies conducted in Ghana [14][15][16] but lower than a prevalence rate of 16.7% in rural Ghana [17], and the national prevalence of 12.3% among pregnant women in the country [18]. Tis points to increased chances of the transmission of some STBBIs from mother-to-child (MTCT) and maternal complications due to infections. Timely screening, administration of immunoprophylaxis, vaccination, and education on STBBIs are required for expectant mothers.
Te seroprevalence of HCV (0.8%) in our study is far less compared to a study in Ghana by Ephraim et al. in 2017 who reported a prevalence of 7.7% [16]. However, comparable lower and higher prevalence is being reported in other parts of Africa including 1.7% in Nigeria [22,[25][26][27][28][29]. Te risk of MTCT of HCV ranges between 5-15%, complicated by the unavailability of protocols to determine viraemia levels in seropositive mothers. Vertical transmission of HCV is near zero in mothers negative for HCV RNA but 4-15% in HCV RNA-positive mothers [30]. Despite the low prevalence of HCV in this study, the introduction of further testing to determine the viraemia levels of seropositive mothers will help avert MTCT in Ghana.
Te 0.8% prevalence of HIV recorded among pregnant women in our study is comparably higher to 0.6% obtained in a rural setting in Ghana [17] but lower compared to the prevalence reported in some urban areas [31,32]. In southwestern Nigeria, and some parts of Africa, a study among pregnant women revealed higher HIV prevalence [29,31,33] but lower in Cuttack, India (0.5%) [34]. With the advances made in antiretroviral therapy, infected mothers can be managed to efectively prevent MTCT and lessen the economic burden due to HIV morbidity and mortality in both mothers and babies.
Syphilis is one of the curable infections in pregnancies but with adverse complications if undiagnosed or untreated. Congenital syphilis is the ramifcations of maternal syphilis  that is undiagnosed, inadequately treated, or untreated [35]. Te 0.8% seroprevalence in our study is lower than reported in similar research works in Ghana, Nigeria, Ethiopia, and Sudan [36][37][38][39][40] but higher than 0.24% obtained in Ho, Ghana, and 0.19% in Portugal [32,35]. Despite the low prevalence in our study, it still remains a public health concern due to its adverse efects on newborn. Te knowledge of the pregnant women on STBBIs was good with 66.3% cognizant of MTCT of infections. Te knowledge of MTCT of infections is comparably higher than a similar study which recorded a 34.7% knowledge level [41]. Health promotion activities of early preventive strategies, healthy lifestyle, and well-being should equally be directed at raising community awareness of syphilis and hepatitis in the study area.
Te univariate risk factors associated with and predictive of the occurrences of the STBBIs were FGM and gravidity. Also, a family history of HBV was found associated with HBV infection in the study. Family history of hepatitis [15], history of close contact with hepatitis patients [42], and  [43]. A study in China associated low rate of HIV infection in patients vaccinated against HBV [44]. Not all, mothers' completion of the hepatitis B vaccination schedule was protective against infection with HBV during childhood [45]. Tese fndings imply a protective role of HBV vaccination and reduced risk of some STBBIs as we found no infection among participants vaccinated against HBV in this study. Female genital mutilation (FGM) involves removing fesh from the private part of woman. Te national prevalence is estimated to be 11.7% [46]. In the Upper West region where this study was conducted, the prevalence is estimated at between 41.1% and 50.5% [46,47]. Aside from the adverse efect of FGM on sexual satisfaction, the risk of HBV, HCV, and HIV among FGM victims might be attributed to the greater percentage (84%) of the cases carried out by traditional practitioners locally called "wanzams" [47]. Our study found that 23.0% of pregnant women had experienced FGM. Females with FGM have a lower sexual function index compared to their uncircumcised counterparts [48] resulting in dryness and bruises during sex increasing the risk of blood-borne infections. Other efects that increase the risk of infection include open sores and bleeding [49] associated with FGM. With regards to sexual behavior, circumcised women are less likely to decline sex and demand condom use than uncircumcised women as reported in a study in Kenya [50] which could increase their risk of contracting STBBIs.

Conclusion
In our study, FGM was a strong risk and predictive factor of STBBIs among pregnant women in Jirapa municipality. Concerted eforts to terminate the practice of FGM in the study area and the augmentation of an integrated cultural approach in the improvement of reproductive health practices are recommended by all stakeholders.

Data Availability
Te data supporting the current study are available from the corresponding author upon request.

Additional Points
In low resource settings, a lot of cases of HBV and HCV infections are thought to be through congenital infection. Tis risk factor could not be assessed in our study. Also, there are many infections classifed as STBBIs. However, only HCV, HBV, HIV, and syphilis were studied and cannot be generalized for all STBBIs.

Conflicts of Interest
Te authors declare that they have no conficts of interest.

Authors' Contributions
EDK, GM, AA, NS, and JBZ conceptualized the idea for the study, data collection and analysis, and drafting of the manuscript. WW, EKV, and SK contributed in manuscript development and data analysis. Tis work is part of thesis supervised by EDK at the University for Development Studies.