Introduction

Infection with hepatitis B virus (henceforth HBV) is a serious global health problem with significant morbidity and mortality [1]. The overall global burden of HBV remains enormous [2]. HBV is a partly double-stranded DNA [3], which is transmitted through contact with infected blood and body fluids [4]. The virus remains infectious for long periods on surfaces [5].

Moreover, HBV infection is highly variable in both presentation and severity: about 70% of acute infections in healthy adults are asymptomatic, while the remaining 30% of patients have symptoms such as fever, malaise, anorexia, nausea, vomiting, diarrhoea, abdominal pain and jaundice [6]. Elevated alanine transaminase levels, presence of hepatitis B surface antigen and hepatitis B core antigen are characteristic of acute infection [3]. On the other hand, chronic hepatitis B features the persistence of hepatitis B surface antigen for more than 6 months [7]. HBV replication induces hepatic inflammation and progression of liver fibrosis [3].

The 5-year cumulative incidence of cirrhosis ranges from 8 to 20% in untreated patients with chronic HBV, and that of hepatic decompensation is 20% among cirrhotic patients [7].

HBV is an oncogenic virus [8], that is, its DNA can integrate into the host hepatocyte genome, promoting the development of hepatocellular carcinoma (HCC) [9].

HBV accounts for more than half of primary liver tumours cases worldwide [10]. HCC develops in about 20% of non-cirrhotic patients, while the annual risk of HCC in cirrhotic patients is 2 to 5% [7, 9]. Therefore, it is essential for primary care providers to play an active role in the screening, diagnosis and management of HBV [11]. Such preventive measures constitute a major component of the management of HBV infection [12].

Despite the fact that vaccination remains the most effective prevention method of HBV [13], more attention should also be paid to general education and specialized courses for protection of high-risk groups [14]. High-risk groups for HBV infection include intravenous drug users, infants born to infected mothers, males who have sexual intercourse with other males, haemodialysis patients, healthcare workers and household contacts with HBV-chronic patients [15].

To that end, the World Health Organization (WHO) goals include 90% complete coverage of HBV vaccination, a reduction in the prevalence of HBsAg in children < 5 years of age to 0.1% and an improvement in the rates of treatment to 80% by 2030 [16]. Besides, better understanding of the epidemiology and burden of HBV, its main routes of transmission, the high-risk groups and natural history of the disease is pivotal for its management [17]. This study aims to assess the prevalence of HBV in Egypt, analyse the demographic characteristics of HBV infected patients and trace the most common routes of transmission, all in relation to the current Egyptian preventive measures.

Methods

Study design and data source

This study was based on the data from the most recent Egyptian Health Issues Survey (EHIS) which was conducted by El-Zanaty and associates in 2015 [18]. The EHIS was administered by the Egyptian Ministry of Health and Population (MOHP) and funded by the United States Agency for International Development (USAID), which focuses on the most challenging health issues, namely, blood-borne viruses, non-communicable disease (NCDs) risk factors (hypertension, smoking and obesity) and maternal and reproductive health.

Sampling and data collection

The study design of EHIS was the same as that of the Egyptian Demographic and Health Survey-2014 (EDHS) to investigate different health indicators [19]. In both EDHS and EHIS, a nation-representative sample was calculated in multistage stratified sampling. Stratification and primary sampling units (PSUs) were based on the most recent census carried out by the Egyptian Central Agency for Public Mobilization and Statistics (CAPMAS); each Shiakha (an urban neighbourhood unit) or village represents a primary sampling unit (PSU). The EDHS had a representative sample of 842 PSUs, while EHIS enrolled a subsample of 614 PSUs from the selected list of PSUs for EDHS. Figure 1 provides a detailed description of the sampling technique [18].

Fig. 1
figure 1

Flow chart of the study

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Participants

The data of a total sample size of 16,671 participants aged 15–59 years old who agreed to participate in the EHIS were included; the participants who did not agree to perform the hepatitis B tests or had missing results (n = 677) were excluded. The inclusion criteria for EHIS were that individuals aged 15–59 who were usual residents or present in the EHIS sample households on the night before the EHIS interviewer’s visit were eligible for a detailed interview on a range of health issues.

Outcome variable: hepatitis B result

Procedures for testing

Testing for HBV

Screening using hepatitis B surface antigen test (HBsAg) followed enzyme-linked immunosorbent assay (ELISA) technique, which is a reliable test of apparent HBV infection; individuals with a positive HBsAg result had an active HBV infection. A sample of seven millilitres of venous blood were obtained from each participant. Samples were stored in ethylenediaminetetraacetic acid (EDTA) vacutainer tubes with a unique pre-printed barcode identification number (ID). These samples were collected temporarily in field laboratories where they were centrifuged, and the obtained plasma samples were stored in liquid nitrogen tanks using the same ID coding system. The testing procedure was completed in the Egyptian Central Public Health Laboratory (CPHL). Retesting of 10% of samples in CPHL and 5% in Theodor Bilharz Research Institute was conducted for quality assurance.

Criteria for classification

HBsAg test, which detects the presence of hepatitis B surface antigen in the blood, was used to identify individuals with an active hepatitis B infection. Based on the laboratory results, study participants were categorised into HBV positive group “if tested positive to HBsAg test” and HBV negative group.

Predictor variables/determinants

Based on the literature review and available data, the following predictors/risk factors for having hepatitis B positive results have been selected for analysis:

  • Demographic variables (age, gender, marital status, residence, education level, work, religion, and smoking)

  • Medical/ surgical procedures: history of hospitalization, stitches, catheterization, dialysis, endoscopy, surgeries, blood transfusion, intravenous lines or injections and schistosomiasis injections

  • Dental interventions of any kind

  • Complementary and alternative medicine (CAM) techniques: acupuncture and cupping with or without blood

  • Circumcision: we combined data on both male and female circumcision into a single variable and included another variable about who did the circumcision

  • Barbers and beauty salons services: hair salons and barber visits frequency and whether the participant uses his/her own utilities or the shop utilities

  • Tattooing and ear-piercing

Ethical considerations

Ethics approval for EHIS was obtained from the Research Ethics Committee of the Ministry of Health and Population (MOHP). Informed consent was signed by all participants prior to serological testing for HBV. A permission was also granted from DHS to conduct this analysis. Patients with positive HBsAg were referred to special centres for further assessment and treatment, if needed.

Statistical analysis

Data were retrieved from demographic health survey (DHS) website and analysed using Stata® (version 16), considering significant level of P ≤ 0.05. Descriptive statistics were presented in the form of frequency tabulations for categorical variables and summarized by mean/median and SD/IQR for continuous variables. Complex survey design was incorporated in all analyses considering sample weights, strata and primary sampling units. Bivariate association between categorical variables was conducted using the chi-square test with reporting of the Scott-Rao χ2; only variables with significant association on the bivariate tests were entered in the unadjusted and the adjusted logistic regression models.

Results

The total number of eligible populations included in this analysis was 16,004. The following are the main characteristics: age range and mean (± SD) age was 15–59 and 33.5 (± 12.4) years respectively. 55.2% (n = 8838) were females and 44.8% (n = 7166) were males. Most participants (68.7% (n = 10,776)) were married, while 27.2% (n = 4345) were never married. Over a half of participants (51.8% (n = 8295)) lived in rural areas, while 48.8% (n = 7709) lived in urban areas. More than half of the study population had secondary school level education (56.9% (n = 9175)), while 15.0% (n = 2396), 12.7% (n = 2027) and 15.0% (n = 2406) had no education, primary school education and college level education, respectively. Most of the study population (79%, n = 12,642) were non-smokers, while 20% (n = 3362) were everyday smokers.

Overall, 1.52% (n = 277) tested positive in the final HBV test, representing the prevalence of HBV. The bivariate association of HBV results and participant characteristics are illustrated in Table 1: gender, marital status, job status and smoking have significant association with positive HBV test. Interestingly, HBV prevalence was higher with older age groups, but this was marginally statistically insignificant (P = 0.0546). The mean (95% CI) age of HBV positive participants was 37.4 (35.6–39.1) and was statistically significant higher than the mean (95% CI) age of hepatitis B negative participants which was 33.5 (33.3–33.7) by adjusted post estimation Wald test of difference of survey means. Figure 2 provides further illustration of the distribution of prevalence of hepatitis B across age groups and gender, while Table 2 shows the association of HBV prevalence and medical and surgical procedures, circumcision, acupuncture, cupping, tattooing and barbershop and beauty salons; of these exposures, cupping “with and without blood” injection for treatment for schistosomiasis and endoscopy were associated with HBV infection.

Table 1 Description of the studied population (n = 16,004)
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Fig. 2
figure 2

Prevalence of hepatitis B by age group and gender

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Table 2 Bivariate association between procedures and practices and hepatitis B final result (n = 16,004)
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Table 3 shows predictors of HBV infection status in unadjusted and adjusted regression models. In the former, age groups, gender, marital status, job status, smoking cigarettes, receiving cupping, and receiving injection treatment for schistosomiasis were significant predictors for HBV infection; in the latter, married participants compared to participants who never married were more likely to have HBV infection (OR 1.97; 95% CI 1.04–3.5) and who did not receive cupping without blood had 83% less odds of HBV infection compared to those who did (OR 0.17; 95% CI 0.05–0.59). Participants who did not know if they had schistosomiasis injection therapy were more likely to have HBV infection, compared to participants who had a history of receiving injection therapy for schistosomiasis (OR 4.73; 95% CI 1.39–16.12).

Table 3 Unadjusted and adjusted logistic regression of the association of hepatitis B result and risk factors
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Discussion

HBV is a highly infectious blood-borne pathogen [17]. According to WHO, there are about 257 million people living with chronic HBV in the world, and there were an estimated 887,000 deaths in 2015 mostly due to cirrhosis and hepatocellular carcinoma [20]. The chronicity of HBV, in addition to its hepatic and extrahepatic complications, makes it a global target for elimination. In 2016, the United Nations announced the 2030 sustained development goals (SDGs), and WHO adopted a global viral hepatitis strategy adopted by member states targeting the elimination of viral HBV by 2030 [21].

Despite the tremendous Egyptian efforts in the management of hepatitis C virus (HCV), elimination of HBV has yet to gain much traction. In this study, the prevalence HBV is 1.52%, while in 2015, it was 6.3% [22, 23]. The higher magnitude of the HCV problem in Egypt has masked the HBV dilemma. In 2018, Egypt launched a mass campaign for the screening of and treatment for HCV. All Egyptian adults were eligible to be enrolled in this campaign [24]. The model of mass testing and treatment is one of the most effective pillars of disease elimination. It has been tried with other infectious diseases such as Malaria [25]. According to a German report by Krauth, mass screening, however, is not cost effective in diseases with low prevalence [26], and so mass screening of HBV− unlike HCV− was not a priority in Egypt.

HBV is a preventable disease. Introduction of the highly effective recombinant HBV vaccine has led to a significant decrease in HBV incidence [27]. HCV and HBV have common routes of transmission; therefore, it is believed that mass campaigns for schistosomiasis treatment in the 1980s led to increased HBV transmission as well as HCV [28]. However, this was not evident in our study as only individuals who did not know about their history of anti-schistosomal treatment were significantly representative in the positive group (P value 0.016; OR 4.73; 95% CI 1.39–16.12). Developing a unified plan for prevention of blood borne pathogens could aid in the elimination of both HCV and HBV.

The Egyptian plan to control viral hepatitis began in the early 1990s with screening of blood donors [29]; then, in 1992, Egypt added HBV vaccine to the Egyptian compulsory list of vaccination [27]. Subsequently, Egypt launched a preventive infection control plan to promote safe practices in hospitals and health care facilities in 2003. It was a nationwide plan to increase awareness, implement infection control measures in healthcare facilities and train healthcare workers [29].

For the sake of developing an effective plan for HBV elimination in Egypt, we need first to understand the characteristics and risk factors of HBV in Egypt. Our demographic analysis of EHIS revealed a higher prevalence of HBV among older population. Despite the marginally statistically insignificant difference between both groups (P value 0.0546), the mean age of HBV positive participants was greater than HBV negative participants (37.4 versus 33.5 years, respectively). This is likely due to the existing preventive measures and the campaign of compulsory HBV vaccine that started 30 years ago [29]. Egyptian males are also more liable to have HBV than females. Males have lower hygienic measures than females [30,31,32], larger proportion of people who inject drugs (PWID) [33] and, finally, Egyptian females have lower risk for HBV exposure due to higher proportion of unemployed females in Egypt which is furtherly reflected in the high significant difference between both groups regarding work status (P value <0.001) [34].

These findings relate to other national [23, 35, 36] and regional studies [37, 38]. The Egyptian report of sentinel acute viral hepatitis surveillance revealed a high prevalence of HBV among urban populations, yet this was not significant in our study (P value 0.07) [39]. Education level also did not show any significant difference between both groups despite the reports that associate higher education levels and good health [40, 41].

According to a meta-analysis conducted in 2014, smoking is an additive effect to HBV and HCV for the development of hepatocellular carcinoma [42]. A notice that needs a great attention as 20% of the selected sample from EHIS gave a history of smoking and there is a significant prevalence of HBV among Egyptian smokers. HBV can be transmitted through body fluids (e.g., seminal and vaginal fluids)” [43, 44] and that may explain the higher incidence of HBV among the married individuals (P value 0.002; OR 1.97; 95% CI 1.04–3.5). Some reports linked between some religious rituals and spread of blood-borne pathogens such as mourning blades in Shiite population [45]. Fortunately, these behaviours are not present in the Egyptian religious behaviours either in Sunni Muslims or Christians; thus, there is no statistical difference in HBV prevalence in Egypt regarding religion (P value 0.974).

The Egyptian prevention plan has achieved success in deterring the major causes of HBV transmission. Both study groups were comparable regarding performing all medical and dental procedures such as surgeries, hospitalization, insertion of intravenous lines and history of injections (P values 0.409, 0.977, 0.791 and 0.989 respectively). There is a statistically significant difference between both groups regarding history of performing gastrointestinal endoscopy (P value 0.0539). Screening for oesophageal varices is recommended for cirrhotic patients. Transmission of HBV through improper disinfection of endoscopes is possible due to the low infective viral load but it is not common in medical practice due to the major advances in disinfection techniques [46, 47].

Unsafe blood products remain a huge threat to spread HBV. This is supported by a WHO regional office of Eastern Mediterranean region (EMRO) report that stated that there are many countries in the region who still depend on the non-sensitive rapid diagnostic kits and that there are only 13 of the 22 countries in the region participating in an external quality assessment program [48]. The Egyptian efforts in the screening of blood donors’ programs have led to an advanced control of HBV transmission through blood products as evident in the non-significant differences between both groups regarding the history of blood transfusion (P value = 0.17).

Because the application of CAM is rising in Egypt, there are several arguments regarding its safety, efficacy, and the evidence-based rationale. Malpractice and inexperienced professionals are main issues that need to be solved [49, 50]. These CAM techniques could be hazardous if applied in poor infection control measures and that could explain the significant difference between both groups regarding history of cupping with or without blood (P values 0.016 and < 0.001 respectively). Moreover, using an adjusted regression model, individuals who did not receive cupping without blood are less likely to have HBV infection than individuals who gave history of receiving cupping without blood (OR 0.17; 95% CI 0.05–0.59).

Female genital mutilation (FGM) is a global healthcare problem that affects women’s sexual and reproductive health; therefore, a global call to ban FGM has been launched. In Egypt, FGM has been criminalized since 2008, leading to a drop in FGM rate in Egypt from 94 to 88% in 2015. Over half FGM were performed by a physician or nurse rather than a traditional practitioner [51, 52]. Unlike FGM, male circumcision may have a beneficial effect on man’s health. It is prevalent in 94.7% of Egyptian males [53], and this high prevalence of circumcision in both genders may have led to insignificant difference between both groups (P value 0.066).

Barber and beauty salons services are also possible risk factors for blood-borne infections and poor knowledge of the barbers could aggravate the problem [54, 55]. Increased health awareness is mandatory for better disease control. Campaigns that encourage the use of disposable tools are highly recommended. Our findings coincide with those from a recent systematic review [56] that there is no association between hair and nail salons and the risk of HBV and HCV. Furthermore, despite the insignificant differences between both groups regarding tattooing, ear-piercing and going to barber/beauty salons, continuous follow-up and awareness campaigns need to be organized for better outcome.

These findings project an authentic image for HBV and its major risk factors in Egypt. This image can be a cornerstone in HBV elimination plan in Egypt. Still, new plans need new actions: new treatment guidelines, screening campaigns to highly susceptible groups such as HIV patients, PWID, hospital admissions of pregnant females to reduce-mother-to-child transmission and the use of single-use syringes as well as introduction of harm reduction policies to be implemented in the health system.

However, this study is limited primarily by its cross-sectional design, which precludes detection of a causal relationship between covariates and HBV infection. In addition, we were able to analyse only previously known risk factors.

In conclusion, Egypt has taken considerable steps to combat HCV. Still, there is a long way toward the elimination of HBV. EHIS revealed that the previous Egyptian control plan for viral hepatitis achieved success in controlling many risk factors. This study recommends the implementation of special screening programs to highly susceptible patients and treatment optimization as crucial steps for HBV elimination.