Burden of hepatitis B surface antigen sero-prevalence and associated factors among pregnant women receiving antenatal care at a public health institution, southern Ethiopia, 2018: implications for public health prevention

Introduction

Hepatitis B is a serious liver infection in humans caused by the hepatitis B virus (HBV). The estimated incubation period from time of exposure to onset of symptoms is 6 weeks to 6 months [1]. HBV is mostly found in the blood with lower concentrations in other bodily fluids, including saliva, semen, and vaginal excretions [2]. HBV is more infectious and more stable in the environment than other blood-borne pathogens (e.g., human immunodeficiency virus (HIV)) [3]. HBV is transmitted through exposure to infected blood, semen, other bodily fluids, or is transmitted from infected mothers to their infants during pregnancy. Other sources of HBV transmission may occur through sexual intercourse and exposure to contaminated blood [1]. Moreover, mother-to-child transmission (MTCT) is believed to be the most important mode of transmission in regions with intermediate to high HBV prevalence rates. Infants born to untreated HBV-infected mothers can acquire infection from the mother, mostly during birth [4]. Infants born to pregnant mothers who test positive for both hepatitis B surface antigen (HBsAg) and hepatitis B e-antigen (HBeAg) have a 70–90% risk of becoming infected and about a 10–40% risk if they test positive for only HBsAg [5, 6]. The risk of HBV transmission decreases in settings where there is periodic perinatal HBV screening, immune prophylaxis given to infants born to HBV-infected mothers, and hepatitis B vaccination administration both to high-risk mothers and all newborn infants [7, 8].
The World Health Organization (WHO) has provided detailed guidelines for the prevention, care, and treatment of HBV. HBV vaccinations can prevent 70–95% of HBV infections in infants born to HBeAg and HBsAg positive mothers [7]. Without necessary intervention, the risk of vertical transmission is between 40% and 90%, leading to the development of a chronic infection which predisposes infected persons to liver cirrhosis and primary hepatocellular carcinoma (HCC). It is also evident that viral hepatitis during pregnancy is associated with a high risk of maternal complications [8]. HBV infection is a serious global health problem with 2 billion people infected worldwide and 257 million suffering from chronic HBV infection [1, 4]. Of those infected, a majority of these individuals acquired the infection during the prenatal period and early childhood. Without necessary interventions, the risk of vertical transmission is 40–90%; it is evident that viral hepatitis during pregnancy is associated with high risk of maternal complications [9, 10]. In Africa, HBV remains a major cause of morbidity and mortality [11]. The risk of becoming a chronic HBV carrier is 90% [1] with up to 50% of HBV carriers dying of complications, including liver cirrhosis and HCC [3]. The WHO considers HBV as the second leading cause of malignancy next to tobacco among carcinogens [7] which also develops into a chronic infection that predisposes infected individuals to liver cirrhosis and primary HCC [3].
Chronic HBV in Ethiopia was estimated at 7.4% from a 2016 report conducted in Ethiopia [11]. Based on the WHO classification (> 8%), the country is considered a high prevalence region implying an immediate public health priority. According to a systematic review and meta-analysis study conducted in 2018, the overall prevalence of HBV among pregnant women in Ethiopia was 4.7% [12, 13]. This might include universal antenatal screenings of pregnant mothers for HBsAg and vaccination of their babies at birth, yet it is not a routine practice in most health settings in Ethiopia [14]. Despite these screening attempts, Ethiopia is among countries with high intermediate prevalence of HBsAg (5–7.99%) globally [3]. Previous studies conducted in Ethiopia showed the prevalence of viral hepatitis B ranged from 3.5 to 7.8 [14–32]. The studies suggested that socio-demographic factors, such as education level, residence, marital status, history of abortion, history of sexually transmitted infection, multiple sexual partners, history of dental procedures, and different cultural practices, such as scarification and nose piecing, are associated with HBsAg seroprevalence. The prevalence of HBV infections varies markedly in different geographic areas of the world, in different population sub-groups, as well as with time and routes of transmission [16]. However, few studies have been conducted on the public health issues affecting these vulnerable populations, and there is limited information on the HBsAg seroprevalence among pregnant mothers in southern Ethiopia.

Aim of the research

Therefore, this study aimed to measure the burden of hepatitis B surface antigen sero-prevalence and associated factors among pregnant women receiving antenatal care at a public health institution, southern Ethiopia, 2018.

Material and methods

Study design, setting and duration of the study

A hospital-based cross-sectional study was conducted from May 1 to 30, 2020 at the Jinka Hospital. Jinka Town is the capital of the south Omo zone in southern Ethiopia, which is located at a distance of 345 km southwest of Arba Minch. Jinka Town has an estimated total population of 22,475 people with 10,701 women and 11,774 men. The town has one hospital, two health centers, and 11 private clinics. Annually, an estimated average of 3,000 pregnant women visit the antenatal care (ANC) clinic for routine pregnancy check-up services that include the assessment of pre-existing health conditions, vaccinations, nutrition counseling, micronutrient supplementation, and early detection of pregnancy-related complications.

Study population

The source population consisted of pregnant women who visited the antenatal care unit at Jinka Hospital during the study period and fulfilled the selection criteria. The inclusion criterion was confirmed pregnancy. Pregnant women who were critically ill, unable to answer questions, women on HIV treatment with lamivudine, and women who were vaccinated against HBV were excluded from the study.

Sample size and sampling procedure

The sample size (n = 435) was statistically calculated based on the single population proportion formula by taking a 4.3% HBsAg seroprevalence from a previous study [15], desired precision of 2%, 95% confidence level, and 10% non-response rate. Pregnant women who attended the ANC clinic gave consent to participate in the study and were then enrolled until the desired sample size was attained.

Data collection

We used a pre-tested, structured questionnaire to collect socio-demographic, clinical, and risky behavior information. Clinical information, including history of hospitalization and admission, was abstracted from the participants’ medical charts. Following the interview, approximately two milliliters of venous blood was collected from each consenting study participant by a trained laboratory technologist. The blood was processed according to the standard operating procedures, and serum was separated and stored at −20°C prior to assay. Finally, the serum was tested for HBsAg using an ELISA test kit (DIALAB) at Jinka National Blood Bank Center Laboratory strictly following the manufacturer’s instructions.

Data Quality Assurance

To ensure the quality of the data, the questionnaire was first prepared in English, translated to Amharic, and then re-translated to English by a translator fluent in both languages in order to check for accuracy. To guarantee that the questionnaire was appropriate and understandable, it was pre-tested on 5% of pregnant women at Gather Hospital, which is located 27 km southeast of Jinka Town. Training was provided to supervisors and data collectors over one day. The data collection process was supervised, and the collected data were reviewed and checked for completeness by the principal investigator. Collected data were checked for consistency and accuracy. Standard operating procedures were strictly followed during blood sample collection and storage as well as analytical processing. Storage conditions and expiration dates of reagents were checked.

Ethics approval and consent to participate

Ethics clearance was issued from the Institutional Review Board of Arba Minch University. All study participants were informed about the study and assured about the confidentiality, protection, and anonymity of data. After obtaining written informed consent prior to data collection, participants were voluntarily enrolled in the study. Laboratory results of HBsAg were referred to the health facility for further management of infected pregnant women. All HBsAg sero-positive mothers were referred to a physician, received liver function testing via the hospital’s laboratory, and were given supportive care.

Statistical analysis

Data were entered into Epi-Data version 3.1 and transferred to SPSS version 21 for analysis. Descriptive statistical tests, such as proportion and means, were used to compute the socio-demographic and behavioral variables, other explanatory variables, and the outcome variable. Binary logistic regression analysis was used to determine the association between explanatory variables and the outcome variable with odds ratio and 95% confidence interval (CI). All explanatory variables with p-value < 0.25 in the bivariate analysis were included in the multivariate logistic regression model. P-value < 0.05 in the multivariate analysis was considered statistically significant. Multicollinearity between the independent variables was checked using the variance inflation factor. Finally, model fitness was completed using Hosmer and Lemeshow statistics – c2 and p-value.

Results

A total of 422 pregnant women participated in this study, giving a response rate of 97%. The age of the respondents varied between 16 and 38 years with the mean age of 25.50 ±4.8 years. Regarding their marital status, 415 (98.3%) respondents were married and 289 (68.5%) of the respondents were urban residents. One hundred eighty-five (43.8%) of the respondents had an education above secondary level, and 203 (48.1%) respondents were housewives (Table 1).

HBsAg seroprevalence

The overall HBsAg seroprevalence was 9% (38) 95% CI (6–12%) among pregnant women. Further prevalence was disaggregated by age (63.2%), residence (60%), marital status (100%), and occupation (25%) (Table 2).

Factors associated with HBsAg seroprevalence

After adjusting for the effect of confounding variables using multivariable logistic regression at p < 0.05, HBsAg seroprevalence among pregnant women who had scarification were four times more likely to be infected than their counterparts (AOR = 4.43, 95% CI: 1.78–11.06). Those with a history of multiple sexual partners were four times more likely to be infected (AOR = 4.70, 95% CI: 1.66–13.29). Similarly, pregnant women with history of a sexually transmitted infection were 5.5 times more likely to acquire HBV than those who had no history of a sexually transmitted infection (AOR = 5.57, 95% CI: 2.35–13.17), which is highlighted in Table 3.

Discussion

Our study assessed HBsAg seroprevalence and associated factors among pregnant women receiving antenatal care at a public health institution in Jinka in southern Ethiopia. The study findings revealed the overall HBsAg seroprevalence of 9%; the level of endemicity per WHO was 8%. Therefore, the region is classified as a highly endemic region [4]. The prevalence from our study is in the same range as other studies from Ethiopia: Deder (6.9%) [16], Harar (6.3%) [23], Gondar (7.3%) [25], Hawasa Referral Hospital (7.8%) [17], Mauritania (10%) [27], Uganda (11.8) [28], Bua Health District Cameron (9.7%) [29], and Taiwan (10%) [30]. Our study result is lower than 17.2% reported from Nigeria among pregnant women and 19.5% from the same study in Ghana [31, 32]. This may be due to sample size variation and the time period gap among the studies. Our study also reports a higher prevalence as compared to the following studies in different parts of Ethiopia: 3.7% in Addis Ababa [33], 3.5% in Dwuro [19], 3.8% in Felege Hiwot Referral Hospital Bahir Dar [20], 4.3% in Arba Minch General Hospital [15], and 5.4% in Bishoftu [18]. Our findings are higher than the results of studies conducted in Rwanda (2.4%) [28], Algeria (1.6%) [34], Eritrea (3.2%) [35], Libya (1.5%), and Japan (0.8%) [36]. More than sixteen different ethnic groups with different cultural practices and traditions visit Jinka Hospital. Harmful traditional practices including polygamous marriage, early marriage, arranged marriage, and female genital cutting/mutilation are commonly practiced in southern Ethiopia, which might explain the high prevalence of HBsAg seropositivity in the current study [37, 38]. Furthermore, the variation might be attributed to methodological differences and the level of awareness for risk factors of HBsAg seropositivity. The age of detection of HBsAg seropositivity is one of the major determinants of the prevalence rates of HBsAg. Although it is not statistically significant, in some epidemiological studies on HBsAg, there has been a link between age and HBsAg seroprevalence. This research finding revealed that the prevalence of HBsAg varied across the different age groups. The highest HBsAg seroprevalence was observed among the age group of 24–34 years followed by the ages of 15–24 years. This finding is similar to the study conducted in Dwuro and Bishoftu [18, 19]. A possible explanation for this could be that HBV is horizontally transmitted through blood and other bodily fluids, and these age groups are more likely to be sexually active and therefore have more chance of multiple sexual partners. Another possible reason for a higher prevalence of HBsAg among these age groups could be because they are accounted for in a higher proportion than other age groups in visiting an antenatal care institution within this study setting. However, our study is contrary to a study conducted in India [39].
From our study, pregnant women with scarification were four times more likely to acquire HBsAg compared to their counterparts. This could be explained by the fact that many of these body art practices are done at home, and in most instances, shared equipment is used to conduct the procedure for everyone, therefore increasing the potential for transmission of HBsAg. This study finding is similar to a study performed in Uganda [40]. The findings of this study showed that pregnant mothers who had a history of sexually transmitted infections (STIs) were five times more likely to be infected by HBV compared to those who had no history of STIs. This finding is comparable to those reported from Harar Ethiopia and Nigeria [23, 41]. A possible explanation for this occurrence is that HBV and other STI co-infections can occur since STIs and HBV share the same modes of transmission. Pregnant women with a history of multiple sexual partners were four times more likely to acquire HBsAg compared to those with a single partner. Similar findings were reported from Arba Minch General Hospital, Deder, Dwuro and Harar [15, 16, 19, 23]. This may be because HBV is a bloodborne virus; blood, semen, and other bodily fluids are common sources of infection, with sexual contact serving as a mode of transmission. Thus, sexually active women have a higher risk of being infected, especially those who have a history of multiple sexual partners.

Conclusions

This study determined that there was a high HBsAg seroprevalence among pregnant women in southern Ethiopia, which calls for preventive public health measures. We recommend the establishment of health education programs and awareness campaigns concerning the mode of HBV transmission, high-risk behaviors and methods of prevention, cultural norms, and harmful traditional practices at health facilities during antenatal care visits for mothers. Based on the recommendations from the WHO and national protocols, all pregnant women should be screened for HBV, treated, if necessary, to reduce their viral loads, and infants should be vaccinated at birth with a single-dose hepatitis B vaccine to break the cycle of mother-to-child transmission.

Acknowledgments

We express deep gratitude to the staff at Jinka Hospital for their support and dedication during data collection. We would also like to thank Jinka Blood Bank Center personnel for assisting in serological screening of HBV. Lastly, we are grateful to all our study participants and data collectors. Availability of data and materials – The datasets analyzed during the current study are available from the corresponding author upon reasonable request.

Conflict of interest

The authors declare no conflict of interest.