Prevalence and risk factors of hepatitis B and C virus infections among the general population and blood donors in Morocco

Hepatitis B virus (HBV) and hepatitis C virus (HCV) are among the principal causes of severe liver disease, including hepatocellular carcinoma (HCC) and cirrhosis-related end-stage liver disease. The World Health Organization (WHO) has estimated that there are 360 million chronically HBV infected people and 5.7 million HBV-related cases worldwide [1]. HBV is highly infectious and transmitted mainly via blood, body-fluid contact, and vertical transmission [2]. The hepatitis B surface antigen (HBsAg) in serum is the first seromarker to indicate active HBV infection, either acute or chronic [3]. A hepatitis B vaccine, available since 1982, has a high efficacy in the prevention of HBV transmission [2] and has brought about remarkable changes in the global epidemiology of HBV infection. HCV infection is also common worldwide. It is transmitted in a manner similar to HBV and it is estimated that about 3% of the world’s population carry HCV, with 3 to 4 million new infections per year [4]. Hepatitis C is generally asymptomatic, with a strong tendency (up to 80%) for progression to persistent infection [5]. Chronic HCV infection progresses at a variable rate to cirrhosis in 15 to 20% of patients, who then have a 1 to 4% annual risk of developing hepatocellular carcinoma in 20–30 years [6].

Morocco has been placed by the WHO into the intermediate zone of prevalence for both hepatitis B and C; however the exact number of persons infected is unknown for the reason that no large-scale epidemic data exist to assess the true HCV and HBV infection burden in Morocco. Although a few studies have been carried out, they were affected by a selection bias because most studies are generally based on subjects from risk groups or blood donors with lacking information on children and senior citizens not generally included in as specialized groups [7‐9].

The scarcity of data and the degree to which they are out of date were the main reasons behind a nationwide cross-sectional survey aimed to determine the prevalence and risk factors of HCV and HBV infections in the general population and among blood donors to unravel the true status of viral hepatitis in apparently healthy Moroccan persons and thus provide valuable information about surveillance and estimation.

We report here a cross-sectional study to assess the epidemiology of HCV and HBV prevalence among the general population residing or working in the major Moroccan regions and among blood donors from the Blood Transfusion Center of Casablanca, the largest commercial and densely populated city of Morocco. To the best of our knowledge this is the largest community-based epidemiologic study of HCV and HBV infections from Morocco. The sampling procedure adopted and the high participation rate (97.3%) support the absence of selection and non-response bias, ensuring thus an accurate assessment of the prevalence in our study. Most of the previous researchers in this field were limited due to the selective nature of the survey populations. The descriptive epidemiologic data presented in this study can provide new insight into the contribution of HCV and HBV in the etiology of liver disease in Morocco.

The overall prevalence of HCV infection in the general population in our study is found to be 1.58% and was lower than the prevalence reports from close countries; Algeria (2.5%), Libya (3%) and Egypt (15%-20%) [10‐12]. Our estimate was also too much lower compared to what has been reported in the prior decade by Cacoub et al.[13] in which the estimated HCV infection rate was 7.7%. This result is surely related to the nature of the participants enrolled in the study who were mostly hospitalized patients and those who come for consultation suffering from chronic hepatopathy or with nephrological manifestations. Most HCV-seropositive subjects in the present survey had detectable viremia (70.9%), which is consistent with findings in studies from France (80.6%) and Italy (75.9%) [14, 15].

No statistically significant difference in HCV distribution according to gender was found in our study, which is similar to other reports on community-acquired hepatitis C from United states and Belgium [16, 17], However, higher prevalence was observed in advanced age groups; indeed, no anti-HCV seropositive case was found in 152 subjects in age groups younger than 20 years, nevertheless the seropositivity increased progressively from adults (0.77%) to older persons (3.12%). This can be supported by two major reasons. First, before 1994, anti-HCV screening among blood donors was not conducted throughout Morocco and the association of blood transfusion with HCV seropositivity should not be surprising given that the blood product had not been previously screened for HCV. Second, the higher prevalence of HCV in older people could be attributed to a longer exposure to risk factors for HCV transmission; for instance iatrogenic transmission resulting from inadequately sterilized equipments, inappropriate reuse of supplies, etc. This risk factor is considered the main risk associated with HCV infection in the majority of participants from the general population included in this study. This same risk is the primary cause for HCV transmission in many outbreaks documented in United States and European Union health care [18, 19].

Regarding HBV infection, the overall prevalence of HBsAg was significantly lower (1.81%) than that reported from Algeria (3.6%) and Tunisia (4-7%) [20, 21]. Despite the large number of young in <20 group tested (152 subjects), none was positive for HBsAg, These results indicate that the strong efforts made among youngers have had some success since the HBV infant vaccination was introduced in 1992 and integrated into the national immunization program in 1999, in addition, hepatitis B immunoglobulin and HBV vaccine treatment for newborns of HBV-infected mothers at delivery could also contribute to the significant reduction of vertical or perinatal transmission of HBV.

On the other hand, the age-related prevalence of HBsAg showed a progressive decrease after 50 years (1.71%), so among participants who were older than 50 years, the prevalence of anti-HCV was higher (3.12%) than that of HBsAg (1.71%). This can be probably due to deaths caused by HBV-related cirrhosis and hepatocellular carcinoma in this group [22]. Additionally, it has been reported that HBV-associated HCC occurs approximately 10 years earlier than HCV-associated HCC [23, 24]. Conversely, on the whole, the prevalence of HBV in our study population was slightly higher than that of HCV (1.81% vs. 1.58%). Thus, the comparative incidence of the two viruses is consistent with findings in studies conducted in India, China and Bosnia-Herzegovina [3, 5, 25].

Analysis by gender reveals that, the seroprevalence of hepatitis B among males is significantly higher than that found in females; this data was comparable to other reports [26], and no plausible explanation has been given for the higher rate in males in the general population but probably due to the higher exposure to occupational HBV risk factors in men, or else females clear the HBV more efficiently as compared to males [27].

Our research shows a very low prevalence (two cases among 23 578 personts tested) of hepatitis co-infection comparing with Tunisia (5%) and Egypt (22.5%) [28, 29], these results indicate that the HBV positive patients investigated herein do not have an increased risk of exposure to HCV infection. Although this small sample size of reactive cases does not allow data to be compared with other reports, one Italian study found that rates of dual infection increased with age, and was more common in patients over 50 years of age [30]. In this report, the two cases were male subjects belonging to age groups 20–29 years and ≥50 years respectively. Moreover several authors have reported that HBV can reciprocally inhibit HCV replication [31]; specifically, HBV DNA replication has been shown to correlate with decreased HCV RNA levels in coinfected patients [32]. In another Italian study, coinfected patients had a rate of HCV RNA clearance of 71% compared to 14% with HCV monoinfection [31]. Furthermore, coinfected patients have been demonstrated to have lower levels of both HBV DNA and HCV RNA than corresponding mono-infected controls, inicating that concurrent suppression of both viruses by the other virus can also occur [33].

After all, according to research regarding HBV prevalence, Morocco has been estimated as a moderately endemic area; thus, in a WHO collaborative study on viral hepatitis B in which 20 countries have participated, the seroprevalence were reported was 3.3% [34]. Among barbers and their customers, the positive ratio for HBsAg was found to be 2.0% by Zahraoui et al. in 2004 and 28.0% by Belbacha et al. in 2011 [7, 35]. Comparison of these findings with the HBsAg carrier rate estimated in this exhaustive investigation and our preliminary results published by Sbai et al.[36], shows that the epidemiological picture is changing and that the vaccination program has shifted this trend to low endemicity.

In this study, we also measured over a period of three years, the frequency of HCV and HBV infections among 169 605 voluntary blood donors assumed to be without known or obvious risk factors. 0.62% and 0.96% of subjects were tested positive for HCV antibodies and HBsAg respectively, these results were significantly lower compared with the prevalence observed among the general population reported here. This could be explained by the fact that the volunteer blood donors are a preselected healthy group based on donor questionnaires and physical examination as blood is drawn only from those applicants who appear at low risk of having blood-borne pathogens [37]. Moreover, with regard to HCV infection, this prevalence is considerably lower in comparison with that reported among blood donors in 1998 at the same institution and in 1992 at the Regional Blood Transfusion Center of Rabat (0.70% and 1.56% respectively) [38]. This observation is probably due to the improvement of the effectiveness of the medical selection through self-exclusion from blood donation and medical examination. When the results of the present study were compared with those reported from similar blood donors of other countries, a comparable prevalence of HCV antibodies has been reported in blood donors from Libya (0.69%) and Germany (0.65%) [39, 40]. Studies from Tunisia (1.4 %), Senegal (0.8%) and United States (1.8%) reported higher HCV infection rate [41‐43], whereas Algeria (0.18 %), Spain (0.3%), England (0.1%), Bosnia and Herzegovina (0.27%) showed lower frequency of the HCV antibodies seropositivity in comparison to the present study [20, 44‐46].

Measurement of HBV seropositivity, has revealed that 0.96% of the Moroccan blood donors had HBV infection. This seroprevalence is lower than that reported in Algeria (3.6%), Libya (1.28%), Turkey (1.8%) and Iran (1.07%) [20, 37, 39, 46]. Nevertheless, it is higher than the reactivity rate reported in Rabat, Morocco (0.8%), a US community (0.15%), and Bosnia-Herzegovina (0.78%) [8, 25, 47].

Our study throws light for the first time, on the current epidemiological status of viral hepatitis B and C infections in Morocco among the general population and blood donors. This data shows that the prevalence of HBV and HCV in blood donors was significantly lower than that observed in the general population, which emphasizes that the blood transfusion was not a contributing risk factor for transmission of neither HBV nor HCV infection. The main transmission route in Morocco is still attributed to the nosocomial exposure to contaminated instruments.

The present survey reports that the HCV infection is at an intermediate level of endemicity. It also underlines the decrease of hepatitis B incidence rate compared with previous studies. Even with a moderate prevalence, there may be a large reservoir of HCV and HBV-infected persons in Morocco, which indicates that many people are at risk of developing chronic liver disease related to viral hepatitis, added to the fact that antiviral therapy is not affordable by the vast majority of people in developing countries. Therefore, nosocomial risk prevention as well as health education among population are the main interventions that might help limiting the spread of these blood-borne infections.