Risk factors of hepatitis B virus surface antigen carriage and serological profile of HBsAg carriers in Lomé Togo, 2016

Hepatitis B is an inflammatory disease of the liver characterized by hepatocellular necrosis and caused by a virus belonging to the Hepdnaviridae family [1]. Hepatitis B is a major public health concern across the globe. The World Health Organization (WHO) estimated that approximately 240 million people are infected with the Hepatitis B Virus (HBV) worldwide [2] but only 11% of those who live with viral hepatitis are aware of their serologic status [3]. These individuals are at risk of severe illness and death as a result of cirrhosis or hepatocellular carcinoma (HCC). The viral hepatitis pandemic takes a heavy toll on lives, communities and health systems. In 2013, viral hepatitis was the seventh highest cause of mortality globally. It is responsible for an estimated 1.4 million deaths per year from acute infection and hepatitis-related liver cancer and cirrhosis a toll comparable to that of HIV and tuberculosis. Of those deaths, approximately 47% are attributable to HBV [4, 5]. The majority of hepatitis B infections are in Africa where the prevalence is estimated to be 7.2% (6.2–8.2) [6].

The virus is typically acquired via percutaneous or mucosal exposure to infected blood or other body fluids [7]. Because the virus can also be transmitted from mother to child during delivery and through unprotected sexual intercourse, infection of sexually active adults of reproductive age is particularly concerning. Acute HBV infection is characterized by the presence of hepatitis B surface antigen (HBsAg) and Immunoglobulin M (IgM) against Hepatitis B virus core antigen (anti-HBc IgM). During the initial phase of the infection, which is characterized by a high level of viral replication, the patients are carriers of the Hepatitis B viral antigen (HBeAg). The presence of HBeAg indicates that the subject is highly contagious. Antibodies against HBsAg (anti-HBs antibodies) appear a few weeks later, following which HBsAg is lost. Chronic infection is characterized by the persistence of HBsAg beyond 6 months [8]. The persistence of HBsAg is an important risk factor for development of chronic hepatitis and liver cancer.

A previous study estimated the prevalence of this disease in Togo to be 16.4% among young people (aged 15–24 years) in 2010 [9] it varied significantly with gender, marital status, place and region of residence. In that study, the prevalence was 19.2% among males and 13.9% among females. A study conducted in 2011 at University Hospital of Campus in Lomé found a prevalence of 19.08% with 25% in males and 14.8% in females [10]. In 2015, the estimated prevalence of HBsAg was 4.6% among first-year University students at the University of Lomé [11]. These prevalence figures are higher than the average recorded for the West African sub region highlighting the importance of this public health concern in Togo. Public health authorities have been progressively implementing measures to prevent hepatitis B infection since 2008, as evidenced by the integration of hepatitis B vaccination into the Expanded Program on Immunization (EPI) [12, 13]. A workshop on hepatitis B was organised in Lomé in November 2016. On this occasion, Institut National d’Hygiène of Lomé (INH) organized a free screening campaign during which 476 people were enrolled. Blood samples were collected from participants and tested for the presence of HbsAg with Enzyme Linked Immuno Sorbent Assay (ELISA). Samples which tested positive for HBsAg were further analyzed for HBeAg, anti-HBc IgM antibodies, and antibodies against Hepatitis C virus.

A database was established at the end of this campaign. In this study we present an analysis of that database, focusing on risk factors for HbsAg carriage and serological profiles of people with HbsAg, which are still poorly documented in Togo. The objectives of this study were to identify factors associated with carriage of HBsAg and to describe the serological profile of people with HBsAg in Lomé.

The Kabyè-tem ethnic group membership and knowledge of the serological status before the test, were identified as two independent risk factors associated with HBsAg carriage. Of the infected persons, 13.3% were still infectious, and these were all women from the Kabyè-tem ethnic group. Our findings corroborate the results of a previous study that observed that the regions of highest HBsAg seroprevalence among 15–24 years old individuals were the central region (27.7%) and the Kara region (23.1%), which are inhabited by the Kabyè-tem [9]. This ethnic group is the second largest in Togo. Although Kabyè-tem primarily live in the central and Kara regions, many have moved to reside in Lomé and were thus included in this study. To our knowledge, there has not been a study comparing the socio-economic conditions of members of the Kabyè-tem ethnicity relative to other ethnicities. That belonging to the Kabyè-tem group is an independent risk factor for HBsAg carriage could be explained by socio-cultural or genetic factors. Several studies [14, 15] have described the influence of genetic factors on HBV infection and on the elimination of HBsAg.

The fact that knowledge of serological status was shown to be an independent risk factor indicates that most cases were aware of their serological status compared to controls and that screening for HBsAg was not routinely done in Togolese populations. The cases were probably diagnosed with hepatitis B during clinical manifestations prior to our survey. Statistically significant associations could not be identified between HBsAg carriage and the male gender, transfusion, hospitalization, surgery, tattoos and piercing, or having a parent suffering from hepatitis B. Similar observations were made in a previous study conducted in Nigeria in 2011 [16] and another conducted in Ghana in 2013 [17]. This may be related to the fact that this information was obtained on the basis of statements from study participants, they were not likely willing to disclose this information because of stigma. Also, the sample size was too small for identification of certain risk factors such as transfusion, prior hospitalization, or dental surgery. In addition, it is possible that the fact that blood transfusions, hospitalization, and nursing practices are becoming increasingly safe [2] minimized the rate of hepatitis acquisition via iatrogenic routes.

In the hospital-based Lomé study and the national survey among people aged 15 to 24 years there was a statistically significant difference in the prevalence of HBsAg between the two genders [9, 10]. This discrepancy may be due to our smaller sample size. We also found that vaccination did not have a statistically significant protective effect, this possibly reflects a poor adherence to vaccination schedules.

Of HBsAg carriers, 13.3% also carried HbeAg and were therefore still contagious. Importantly, this population is likely sexually active (median age 28 years) and therefore at risk of transmitting the virus to uninfected individuals [18]. A similar prevalence (13.7%) was found in a study carried out among PLHIV on ART in Lomé in 2011 [19], indicating that the odds of sexual transmission in Lomé have remained high for some time.

The prevalence of hepatitis B and C co-infection was 4.8%, which was higher than the 3.9% value previously reported among untreated HIV patients in Tanzania during 2006 [20]. It is also much higher than the 0.6% previously reported in Ghana among pregnant women in the Ashanti region [17]. It therefore appears that co-infection is a significant issue in Togo.

Three major limitations were identified. The first limitation is that our study did not incorporate risk factors such as unsafe sexual behaviour and type of breastfeeding. The second was the fact that the serological diagnosis of the hepatitis B we used in our study may have not detected occult hepatitis whose prevalence is approximately 5% among HBsAg negative individuals [21, 22]. Our study may therefore have underestimated the association with risk factors. The third was that the pre-existing database from which we used unfortunately, did not include information regarding sexual practices and intravenous drug use by the participants; these important risk factors will be addressed in future studies. Despite these limitations, analysis of this database allowed us to identify factors associated with HBsAg carriage and the serological profile of HBsAg carriers in Lomé in 2016.

Our study showed that Kabyè-tem ethnic group and awareness of hepatitis B serological status are independent risk factors for HBsAg carriage in Lomé. A proportion of 13% of HBsAg carriers in Lomé, were in the contagious phase, implying that the risk of transmission of this disease to sexual partners and close neighbours (parents, nurses, domestic workers) remains high in Togo. Education campaigns to encourage screening and subsidization of the vaccination especially among the Kabyè-tem community (particularly women) will likely promote effective control of hepatitis B in Togo. The Expanded Program on Immunization should be reviewed in order to incorporate introduction of Hepatitis B vaccine earlier during the first hours of life to minimize the risks of mother to child transmission.