Hepatitis B is a major public health problem [1Lavanchy D. Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures. J Viral Hepat 2004; 11: 97-107., 2Mahoney FJ. Update on diagnosis, management, and prevention of hepatitis B virus infection. Clin Microbiol Rev 1999; 12: 351-66.]. According to WHO, the number of infected people is estimated to 2 billion worldwide of which 240 million people are reported to be chronically infected by hepatitis B virus (HBV). There are about 65 million individuals who carry HBV in Africa, with a 25% mortality risk. In sub-Saharan Africa, the prevalence of HBV infection ranges from 9-20% [3Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan Africa: a view from tropical and subtropical Africa. Gut 1996; 38(Suppl. 2): S5-S12., 4Kramvis A, Kew MC. Epidemiology of hepatitis B virus in Africa, its genotypes and clinical associations of genotypes. Hepatol Res 2007; 37(s1): S9-s19.]. This high prevalence is derived from epidemiological data which remain insufficient in this part of Africa.

Chronic HBV carrying can lead to complications like hepatocellular carcinoma (HCC) or cirrhosis, or both [5McMahon BJ. Epidemiology and natural history of hepatitis B. Semin Liver Dis 2005; 25(Suppl. 1): 3-8.]. HBV infection is one of the major causes of death related to cirrhosis and liver cancer [6Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: New estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine 2012; 30: 2212-9.]. Some of the challenges with HBV infection are diagnosis and management [7Raimondo G, Pollicino T, Romanò L, Zanetti AR. 2010 update on occult hepatitis B infection. Pathol Biol (Paris) 2010; 58: 254-7.]. Vaccination is known to have significantly reduced mortality due to HBV infection [8McMahon BJ, Bulkow L, Harpster A, et al. Screening for hepatocellular carcinoma in alaska natives infected with chronic hepatitis B: A 16-year population-based study. Hepatology 2000; 32: 842-6.].

The diagnosis of viral hepatitis B is based on the interpretation of several serological and virological markers. Screening for virus surface antigen (HBsAg) is the most common approach in detecting the infection. HBsAg is reliably present in the acute phase of the infection and its persistence beyond 6 months indicates chronic phase. On the other hand, the e antigen of hepatitis B (HBeAg) shows that the virus is multiplying rapidly with an increased risk of transmission [9Kao J-H. Diagnosis of hepatitis B virus infection through serological and virological markers. Expert Rev Gastroenterol Hepatol 2008; 2: 553-62.].

The efficacy of the vaccine against HBV has been exploited especially in areas where children are most affected with risk of chronicity [10Margolis HS, Alter MJ, Hadler SC. Hepatitis B: evolving epidemiology and implications for control. Semin Liver Dis 1991; 11: 84-92.]. In sub-saharan Africa, various data show horizontal transmission in infants. This mode of transmission is not clearly understood but some studies suggested percutaneous infection through saliva or blood and using of contaminated needles and tribal scarification [3Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan Africa: a view from tropical and subtropical Africa. Gut 1996; 38(Suppl. 2): S5-S12.]. The evolution of HBV infection in sub-Saharan Africa is not well known.

Therefore, there is the need for empirical data, which reflect the situation in Africa to inform WHO since current guidelines are based on studies in Europe and Asia [11Shimakawa Y, Lemoine M, Njai HF, et al. Natural history of chronic HBV infection in West Africa: a longitudinal population-based study from The Gambia. Gut 2015. [Epub ahead of print].]. Towards this end, the present study aimed to assess the prevalence of HBV infection at CHU-C of Lome.

The present study aimed to evaluate the prevalence of HBV infection among individuals tested from 2009 to 2011 in CHU-C of Lome, Togo. During this period, 1,200 individuals were screened for HBV infection through HBsAg detection. Of these, majority were females, a finding which is consistent with recent studies by Navarro, N. et al [12Navarro N, Lim N, Kim J, et al. Lower than expected hepatitis B virus infection prevalence among first generation Koreans in the U.S.: results of HBV screening in the Southern California Inland Empire. BMC Infect Dis 2014; 14: 269.]. This could be due to the 12.5% of women screened under the monitoring of pregnancy (PNA). Indeed, it is observed that female proportions were higher than that of men in the age ranges of 20-29 and 30-39 years. These two age ranges correspond to women of childbearing age. We found that more than half of the study population (58.26%) was represented by young adults (20-39 years). So, they were more represented than the children and adolescents under 20 years (13.0%) and also than people ≥ 40 years (28.74%). This makes sense since 20-39 years age range individuals represent an active workforce which forms a large proportion of the total population of Togo. In this group, we also observed higher number of pregnant women being screened for HBV infection. With regard to clinical indications for the HBsAg tracking, the number of individuals tested during a Systematic Screening (SS) was higher than other clinical indications. Pre-Natal assessment and clinical abnormalities related with the liver were also higher than the rest. As SS means people without symptoms or people with symptoms that are not related to the liver disease, we can explain the high number of this category of population by the awareness of the medical staff about hepatitis B infection. Due to this awareness, the screening of HBsAg is offered to the majority of those who are received in medical consultation even if they do not present any particular risk. We observed that the number of people tested decreased from 2009 to 2011. Many reasons could explain this finding. For example, there has been an awareness in the Togolese population about HBV infection after the implementation of a childhood vaccination program in 2007. Before this time, the vaccination against HBV was not available for all the children. As CHU-C is hosting a vaccination center, parents who bring their children for vaccination also want to be vaccinated. Thus, the medical staff of the vaccination center recommends the screening of HBsAg prior to vaccination. Moreover, the year 2010 was an election year in Togo with some decline in general business. Nevertheless, this last reason does not explain the decrease in 2011.

Worldwide, 2 billion people are known to be infected with hepatitis B virus [13Shepard CW, Simard EP, Finelli L, Fiore AE, Bell BP, Hepatitis B. Virus infection: Epidemiology and vaccination. Epidemiol Rev 2006; 28: 112-25.]. However, data on the prevalence of chronic viral hepatitis B are varied. In some countries in Asian and Western Pacific, the prevalence of HBV infection has been estimated to exceed 10% whereas less than 0.5% has been documented in the United States and Northern Europe [14Custer B, Sullivan SD, Hazlet TK, et al. Global epidemiology of hepatitis B virus. J Clin Gastroenterol 2004; 38: S158-68.]. In sub-Saharan Africa, carrier rates range from 9-20% [3Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan Africa: a view from tropical and subtropical Africa. Gut 1996; 38(Suppl. 2): S5-S12.]. The mean prevalence in our study population is 19.08%. This observed prevalence may not reflect the national prevalence since the study was carried in hospital area. In addition, CHU-C where the study took place is the only reference center for hepato-gastroenterology in Togo and the prevalence seen may be higher than the national prevalence because of referred patients. In HIV infected people, the prevalence of HBV infection ranges from 9.7-12.5% [15Agbenu E, Banla A, Kolou M, et al. Serologic markers used for hepatitis B surveillance in Togo: status report and action proposals. Med Trop (Mars) 2008; 68(6): 621-4.-17Patassi A, Benaboud S, Landoh DE, et al. Hepatitis B infection in HIV-1-infected patients receiving highly active antiretroviral therapy in Lome, Togo: Prevalence and molecular consequences. S Afr Med J 2016; 106(6): 634-9.]. However, higher prevalence was found in specific risk groups such as sickle cell disease patients (20.2%) [18Kolou M, Sawadogo H, Fétéké L, Agbenu E, Issa SAR, Ségbéna A.Y. Évaluation de la protection vaccinale contre le virus de l'hépatite B chez le personnel soignant hospitalier à Lomé. Med Sante Trop 2014; 24: 266-70.] and health care workers (36-56%) [19Segbena A-Y, Prince-David M, Kagone TS, Dagnra A-Y. [Human immunodeficiency virus, hepatitis C virus and hepatitis B viruses in patients with sickle-cell disease in Togo]. Transfus Clin Biol 2005; 12(6): 423-6.
[http://dx.doi.org/10.1016/j.tracli.2005.12.003] [PMID: 16414299] ]. Although the number of females tested was higher compared to males, the prevalence of infected male individuals exceeded that of the female. Xia et al. found considerable variations in the prevalence of HBsAg carrier in different regions and gender in China [20Xia GL, Liu CB, Cao HL, et al. Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B, C, D, and E virus infections in China, 1992. Int Hepatol Commun 1996; 5: 62-73.]. Moreover, the prevalence among first generation Koreans in the U.S is higher in men than women [13Shepard CW, Simard EP, Finelli L, Fiore AE, Bell BP, Hepatitis B. Virus infection: Epidemiology and vaccination. Epidemiol Rev 2006; 28: 112-25.]. In contrast with the decrease number of people being tested from 2009 to 2011, no difference was observed concerning the prevalence of infected people among the years. This was not expected because of the global engagement for vaccination against HBV [11Shimakawa Y, Lemoine M, Njai HF, et al. Natural history of chronic HBV infection in West Africa: a longitudinal population-based study from The Gambia. Gut 2015. [Epub ahead of print]., 21Mahoney FJ, Lawrence M, Scott C, et al. Continuing risk for hepatitis B virus transmission among Southeast Asian infants in Louisiana. Pediatrics 1995; 96: 1113-6.]. Furthermore, in Taipei City, the carriage of HBsAg reduced from 9.8% before the vaccination to 0.6% in children after 20 years of vaccination [22Ni YH, Chen DS. Hepatitis B vaccination in children: The Taiwan experience. Pathol Biol (Paris) 2010; 58: 296-300.]. In US, acute hepatitis B incidence declined, from 8.5 cases per 100,000 populations in 1990 to 1.5 cases per 100,000 populations in 2007, the lowest rate ever recorded [23Daniels D, Grytdal S, Wasley A. Surveillance for acute viral hepatitis - United States, 2007. MMWR Surveill Summ 2009; 58: 1-27.]. We expected that with the recent childhood vaccination program implemented in 2007 in Togo, the prevalence of HBV infection would have decreased. Later studies may be warranted to evaluate the impact of the vaccination program on the prevalence of HBV infection in Togo.

Since the number of tested individuals was higher in the age range of 20-39 years, we next investigated the prevalence of HBV infection among the different age groups. Interestingly, individuals with age range from 20-39 years old were more infected than the children and adolescent and also than older population (p<0.05). The main reason of these differences could be the sexual transmission of HBV. Sexual transmission was shown to be involved in HBV contamination [13Shepard CW, Simard EP, Finelli L, Fiore AE, Bell BP, Hepatitis B. Virus infection: Epidemiology and vaccination. Epidemiol Rev 2006; 28: 112-25., 14Custer B, Sullivan SD, Hazlet TK, et al. Global epidemiology of hepatitis B virus. J Clin Gastroenterol 2004; 38: S158-68.]. The same trend was observed in Romanian adult population (18–69 years) during 2006–2008 [24Gheorghe L, Csiki IE, Iacob S, et al. The prevalence and risk factors of hepatitis B virus infection in an adult population in Romania: a nationwide survey. Eur J Gastroenterol Hepatol 2013; 25(1): 56-64.]. So some people in the 20-39 years old, individuals may present with acute hepatitis that will heal spontaneously. Thus, it is likely that older subjects have cleared the virus, explaining the low prevalence in people over 50 years. Another hypothesis to explain the low prevalence observed beyond 50 years is the death of carriers of the virus because of complications. This will therefore result in a reduction of the life expectancy of infected people. Likewise, in the study of McMahon et al., the prevalence of patients with symptomatic hepatitis increased with age, ranging from 9.5% in those aged under or equal to four years to 33.3% over 30 years [25McMahon BJ, Alward WL, Hall DB, et al. Acute hepatitis B virus infection: Relation of age to the clinical expression of disease and subsequent development of the carrier state. J Infect Dis 1985; 151: 599-603.]. The same trend was observed in the USA and in Greenland [26Wasley A, Kruszon-Moran D, Kuhnert W, et al. The prevalence of hepatitis B virus infection in the United States in the era of vaccination. J Infect Dis 2010; 202: 192-201., 27Borresen ML, Andersson M, Wohlfahrt J, et al. Hepatitis B prevalence and incidence in Greenland: a population-based cohort study. Am J Epidemiol 2015; 181: 422-30.]. Furthermore, Xia et al. reported that HBV infection was significantly increased with age in China [20Xia GL, Liu CB, Cao HL, et al. Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B, C, D, and E virus infections in China, 1992. Int Hepatol Commun 1996; 5: 62-73.].

Other reasons have been advanced to explain the high prevalence in adults than children. It has been suggested that African children are infected at birth, but for some genetic reasons, the tests remain negative for many years before the virus reactivates [3Kiire CF. The epidemiology and prophylaxis of hepatitis B in sub-Saharan Africa: a view from tropical and subtropical Africa. Gut 1996; 38(Suppl. 2): S5-S12.]. The diagnosis of HBV used here is based on the detection of HBsAg which appears early after the contamination and disappears some few months later [28Chiu YC, Liao SF, Wu JF, et al. Factors affecting the natural decay of hepatitis B surface antigen in children with chronic hepatitis B virus infection during long-term follow-up. J Pediatr 2014; 165(4): 767-772.e1.]. In Western countries, viral hepatitis B is relatively less frequent and contamination usually occurs at adult age, while in Asia and Africa, chronic hepatitis B is more common and acquired in the childhood or perinatally [1Lavanchy D. Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures. J Viral Hepat 2004; 11: 97-107.].

In our study, we observed that individuals with clinical abnormalities related with the liver (CARL) are more infected by HBV. HBV was found to be one of the main reasons of developing hepatocellular carcinoma [8McMahon BJ, Bulkow L, Harpster A, et al. Screening for hepatocellular carcinoma in alaska natives infected with chronic hepatitis B: A 16-year population-based study. Hepatology 2000; 32: 842-6., 11Shimakawa Y, Lemoine M, Njai HF, et al. Natural history of chronic HBV infection in West Africa: a longitudinal population-based study from The Gambia. Gut 2015. [Epub ahead of print]., 29Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 2006; 45: 529-38.]. It has been demonstrated that HBV and hepatitis C virus (HCV) can persist as chronic infections and then they can lead to chronic liver disease and hepatocellular carcinoma in the United States [8McMahon BJ, Bulkow L, Harpster A, et al. Screening for hepatocellular carcinoma in alaska natives infected with chronic hepatitis B: A 16-year population-based study. Hepatology 2000; 32: 842-6., 23Daniels D, Grytdal S, Wasley A. Surveillance for acute viral hepatitis - United States, 2007. MMWR Surveill Summ 2009; 58: 1-27.]. Out of CARL, Systematic Screening (SS) tracked more infected individuals than other reason for being tested. This suggests that the prevalence of HBsAg is very high in the general population so that SS could be a good way for tracking infected people as the infection is most of the time asymptomatic. It seems increasingly important to screen the entire population because since about one year, tenofovir became available and accessible to patients in Togo.

Taken together, this cross-sectional study on the prevalence of HBV infection highlighted the age range as well as the best method of tracking HBV infection in Togo. The findings presented will be valuable to epidemiologists and national health workers in the prevention and treatment of HBV infection. Furthermore, we recommend systematic screening of HBV in Togo and other countries in the sub-Saharan Africa in order to throw more lights on the epidemiology of HBV in these regions.