Introduction

Despite the availability of a prophylactic vaccine, hepatitis B remains a major public health problem. Approximately, 900,000 persons die from hepatitis B every year; as such, it is among the leading causes of mortality worldwide [1]. Its causative agent, the hepatitis B virus (HBV), is a partially circular DNA virus belonging to the Hepadnaviridae family. It is a small, enveloped virus responsible for both acute (sometimes fulminant) and chronic hepatitis. Moreover, HBV has oncogenic potential [2]. Chronic HBV infection is widespread [3] and its overall prevalence is 3.2% [4].

Although data on hepatitis B in Africa is scarce, its prevalence is among the highest in the world. More than 80 million people are infected with HBV in Africa [5], representing a prevalence of 6.1% [6]. Furthermore, a high prevalence of hepatitis B surface antigen (HBsAg), exceeding 8% in the general population, is observed in sub-Saharan Africa [7]. Hepatitis B is underdiagnosed on the continent, stemming from the frequently silent nature of chronic HBV infection and a lack of public information on its prevention, risks and consequences. Poor general health and vaccinal coverage also contribute to an increased risk of HBV infection in the population [8], with the risk of developing hepatocellular carcinoma [9].

Testing and access to treatment remain limited in many low-income countries, including those of Africa, despite the high burden of HBV infection frequently observed in them [10]. More than 124,000 Africans die each year from undetected and/or untreated hepatitis [11]. Considering these aspects, population screening for HBV infection is a major challenge along the path toward preventing, treating and potentially eliminating hepatitis B [12].The Global Burden of Disease Study 1990–2019 on hepatitis B reported an all-ages prevalence of 12.4% for the disease in Chad in 2019 [13]. This significant public health issue thus concerns Chad directly and requires active surveillance there. Infected individuals can transmit HBV to others via such biological fluids as blood and sexual secretions. In areas of high endemicity and in the perinatal period, this transmission of HBV may be vertical or horizontal [14]. Non-vertical transmission may occur through blood transfusions, blood exposure accidents for health professionals, the use of non-sterile equipment for tattooing, piercing, acupuncture or intravenous drug use, or unprotected sexual intercourse [15].

Among these latter aspects, unprotected sexual activity and substance use in particular may increase the likelihood of HBV infection among university students, who are generally young and apparently healthy [16]. In addition, a family history of HBV infection, sexual activity and socioeconomic conditions have been reported to be the main risk factors for HBV infection among students in Bangui [17] and asymptomatic adolescents in Nigeria [18].

In the 2000s and with the goal of preventing transmission of HBV during childhood, several sub-Saharan countries began adding the HBV vaccine to their Expanded Programs on Immunization. This includes Chad, where the vaccine was added to its national plan in 2008 [19]. Despite this policy, the prevalence of HBV infection continues to increase, especially in the population over 15 years of age (incidence of 26.46% versus a national incidence of 13.62%) [20]. This aspect could hamper the attainment of National Health Plan targets to eliminate viral hepatitis, water-borne diseases and other communicable diseases by 2030 [21]. Studies on the burden of HBV infection among the student population and factors associated with hepatitis B are limited in this community, making it necessary to conduct studies to guide policies for the prevention of this scourge in Chad. Thus, we aimed to determine the prevalence of HBV infection and identify associated factors among a sampling of students in N’Djamena, the capital city of Chad.

Methods and materials

Results

Socio-demographic characteristics

Of the 457 students who participated in the study, 348 (76%) were male and 109 (24%) female, i.e., a sex ratio (M/F) of 3.19. Their median age was 24 years and a majority (75%) were aged less than 25 years. The majority of the participants were from the University of N’djamena (407, 89%). Also, most were single (348, 76%) (Table 1).

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Table 1. Socio-demographic characteristics of study participants.

https://doi.org/10.1371/journal.pone.0273589.t001

Prevalence of HBV and its associated risk factors

Of the 457 students participating in the study, 68 (14.87% (95% CI = 13.9–21.7%) were positive for HBsAg. Table 2 depicts the percentage of people interviewed who displayed risk factors and the prevalence of HBsAg among them. HBsAg positivity was highest among students living with a family (95.6%, n = 65), followed by students having unprotected sex (65%, n = 44), having multiple sexual partners (57%, n = 39), living in a density of residence of more than two (50%, n = 34), sharing sharp objects (46%, n = 31) and having an HBsAg-positive mother (34%, n = 23). Of the 107 (23%) students who had undergone a screening test for hepatitis B previously, 25 were HBsAg positive (37%) (Table 2).

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Table 2. Prevalence of HBV risk factors.

https://doi.org/10.1371/journal.pone.0273589.t002

Bivariate logistic regression analysis of the factors associated with HBsAg positivity among students in N’djamena, Chad

Logistic regression was used to test the association between HBV infection and the independent variables and to identify risk factors. Considering a p-value <0.30 in bivariate analysis, having an HBsAg-positive mother, a history of transcutaneous medical procedures, age, marital status, a history of drug injection, housing style and a number of roommates were identified as candidate variables for multivariate analysis (Table 3).

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Table 3. Bivariate logistic regression analysis of the factors associated with HBsAg positivity (n = 457).

https://doi.org/10.1371/journal.pone.0273589.t003

Multivariate logistic regression analysis of the of the factors associated with HBsAg positivity among students in N’djamena, Chad.

The odds of HBsAg positivity were found to be 2.03 times higher in students having an HBsAg-positive mother (AOR = 2.11, 95% CI: 1.16–3.78, p = 0.013) in comparison to students not having an HBsAg-positive mother. The odds of HBsAg positivity among students having a history of transcutaneous medical procedures (AOR = 2.97; 95% CI: 1.51–5.76, p = 0.001) was 3.14 times higher than students not having a history of transcutaneous medical procedures. The study showed that students living with a family (AOR = 4.63, 95% CI: 1.50–20.52, p = 0.018) were 4.54 times more likely to be HBsAg+ in comparison to students living alone. In contrast, students aged ≥26 years had lower odds of HBsAg positivity (AOR = 0.41, 95% CI: 0.18–0.85, p = 0.022) in comparison to students aged ≤25 years (Table 4).

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Table 4. Multivariate logistic regression analysis of the of the factors associated with HBsAg positivity (n = 457).

https://doi.org/10.1371/journal.pone.0273589.t004

Discussion

This study assessed the prevalence of HBV and its associated factors among students in the main public university and the main private university in N’Djamena, Chad. Its findings show a prevalence of HBV infection (HBsAg positivity) of 14.87% (68/457). That percentage places our study population in the high prevalence group, i.e., well above the 8% threshold established by the World Health Organization [30].

The HBsAg prevalence found in our study is also higher than the overall prevalence of 12.4% reported for all age groups in Chad, and over those reported for some other population groups in N’Djamena, for example 7.2% in pregnant women [31] and 13.5% in HIV-infected patients [32]. The higher HBsAg prevalence may be due to the fact that students were largely part of a relatively young but not young enough population. Indeed, with an average age of 24±3 years, our subjects most likely did not benefit from vaccination against HBV in childhood as part of the Expanded Program on Immunization introduced in 2008 [19]. Outside of that program, the relatively onerous price of the HBV vaccine is not covered by the current Chadian healthcare system, which acts as a barrier to large coverage in this population.

Moreover, the HBV prevalence found in our population is higher than those reported in studies on students from Togo (4.6%) [26], Cameroon (5.6%) [33] and Ethiopia (11.5%) [34]. It is lower however than that reported in Nigeria (31.5%) [35] and comparable to that reported in the Central African Republic (15.5%) [17].

Currently, Chadian students are not provided with prevention information (e.g. on sexuality, sexually transmitted diseases and risky practices), which most likely plays a part in that high prevalence rate. The environment in which students live may also carry risk factors (presence of drugs, alcohol, sex, etc.) [16] and the students themselves are in a period of life where risk taking may be more common, as compared to other age groups. Furthermore, sex education continues to be a taboo subject in Chadian families.

Of the 107 students (23%) who had already been tested for HBV infection in the past, 25 (37%) tested positive in our study. That finding is consistent with data reported by Halatoko et al. in Togo [27]. Our interpretation is that students who knew they were already infected might have been particularly tempted to participate in the study, hoping to receive treatment or to check their serological status.

Focusing on the management and clinical follow-up for HBsAg-positive students, and encouraging those who tested HBsAg and anti-HBc-antibody-negative to complete the vaccination course are both critical. All participants in our study received information on HBV infection and those who tested positive were referred to health facilities for follow-up.

Our data showed that maternal HBV status was significantly associated with HBsAg carriage among our students, likely explained by mother-to-child (vertical) transmission risks. Results similar to ours were reported in Gambia in 2007, where vertical transmission was responsible for 16% of chronic infections [36] https://www.zotero.org/google-docs/?OBBVqDand in Cameroon, where the risk of vertical transmission was substantial despite birth-dose vaccination [37]. These data confirm the hypothesis that in sub-Saharan Africa, a highly endemic region for HBV, vertical transmission merits as much attention as its horizontal counterpart [38].

Our study reported a significantly higher risk of transmission among students living in families, with a seroprevalence of 95.6% (65/68) in this study group. These results corroborate those obtained in the Central African Republic [17], where intrafamilial transmission was reported to be associated with hepatitis B in students. This association is probably due to contact between HBV-infected family members [39], the exchange of sharp objects and the sharing of personal-use items (those causing skin and mucous-membrane lesions), and a lack of knowledge on the different modes of transmission of HBV. For these reasons, public awareness and systematic screening of those living with infected people are essential.

A history of transcutaneous medical procedures was found to be a risk factor for hepatitis B in this study. This could be due to nosocomial transmission of HBV (resulting from non-compliance with universal recommendations to prevent postoperative infections and cross-contamination of equipment and medical devices) [40].

According to the multivariate analysis, students aged 26 years or more were less likely to be infected with HBV than those aged 25 years or less, suggesting age as a protective factor. Similar results were reported by Tula and Iyoha in Nigeria [35], where participants aged 20–24 years were more exposed than other groups. It is possible that the older students had already been infected during childhood or adolescence but cleared that earlier HBV more or less quickly, and thus did not developed chronic infection. Unfortunately, we were unable to check for anti-HBc antibodies (Ab) to confirm this hypothesis. Similarly, we did not check for anti-HBs Ab, which could have given us an idea of the percentage of vaccinated students.

Strengths and limitations

Our study adds to data regarding prevalence of hepatitis B virus infection in Chad. Such findings are expected to guide public health strategies for the diagnosis of HBV pathologies among students and the general population. Although our work involved a mixed population of students from both the University of N’djamena and Emi-Koussi University, it does have certain limitations. As underlined above, we were unable to carry out total anti-HBc Ab, anti-HBc IgM Ab and anti-HBs Ab testing. This would have allowed for a distinction between subjects who were acutely infected (with anti-HBc IgM Ab), chronic carriers, showing recovery from an acute or chronic infection (anti-HBc Ab positive) [41, 42], or immunized against HBV (anti-HBs Ab positive). The face-to-face nature of our interviews may represent a limitation and constraints in the study design may have introduced selection bias.

Logistic regression was adjusted for other variables but only ten were taken into account. This may represent a limit on the control of confounding factors.

Conclusion and recommendations

Our study showed that the prevalence of HBV infection in students was higher than the overall prevalence in Chad. Having an HBsAg-positive mother, a history of transcutaneous medical procedures, living with a roommate, and living with a family were significantly associated with HBV status. In view of our results, HBV prevention and treatment policies should include: awareness campaigns to inform at-risk populations like students on HBV transmission pathways; HBV vaccination at birth; mandatory full hepatitis vaccination status before children start school; the promotion of mass screening to identify & treat chronic HBV carriers and reduce transmission; reduction of vaccination costs; and the promotion of free-of-charge HBV screening for pregnant women.

Supporting information

Acknowledgments

We thank the laboratory technicians at Hôpital de la Paix in N’djamena who took the blood samples and performed the various tests. We express our gratitude to the survey’s data collectors and supervisors. We furthermore thank the deans of Cheikh Anta Diop University in Dakar for their guidance. We express our gratitude both to the student secretaries who facilitated participation in the study and particularly to the students who joined us for it.