Serological markers of Hepatitis B and C among juvenile immigrants from Albania settled in Greece

Abstract

Background: Greece is a place of settlement for a large number of immigrants, particularly from Albania, which constitute special community groups for public health policies. Objectives: This study was designed to assess the seroprevalence of serological markers for Hepatitis B and C among juvenile immigrants from Albania settled in Greece. Methods: The study population included 504 subjects, 418 males and 86 females, aged 10–23 years old who have emigrated from Albania to Pogoniani-Greece and participated voluntarily in vaccination programmes against Hepatitis B. The serum samples were examined with enzyme immune assays for the immunological markers HBsAg, anti-HBc, anti-HBs and anti-HCV. HBsAg positive samples were further tested for IgM anti-HBc, HBeAg and anti-HBe. Results: Among the examined subjects, 40.5% were found positive for anti-HBc, indicating an HBV contamination. Specifically, 11.7% were carriers of HBsAg, whereas 28.8% were negative for HBsAg but positive for anti-HBc. Only 6.5% was positive exclusively for anti-HBs. The rest (53.0%) presented no positive serological markers. Among the HBsAg positive patients, 8.5% were found positive for HBeAg, while 5.1% was positive for IgM anti-HBc. Finally, only 0.6% of the sample presented antibodies against HCV.

Conclusion: The examined migratory population is described by a high prevalence of Hepatitis B. Therefore, specific public health measures are necessary. However, no data was found that indicate potential public health dangers regarding hepatitis C.

Key words::

• Infectious diseases
• epidemiology
• public health and community medicine
• hepatitis
• immigrants
• seroprevalence

Introduction

Viral Hepatitis B and C continue to constitute severe public health concerns around the globe. According to the World Health Organization (WHO), it is estimated that more than one third of the world's population has been infected with the Hepatitis B virus (HBV) some time in their life and about 5% of the population are chronic carriers of HBV (1). In addition, the WHO estimated that about 3% of the world's population has been infected with the Hepatitis C virus (HCV) and more than 170 million people have a chronic infection (2). The gravity of the problem varies widely with the geographic area. It has been proven that both chronic Hepatitis B and C can potentially lead to liver cirrhosis, hepatic decompensation and hepatocellular carcinoma (3), although each virus is characterized by a different oncogenic mechanism (4,5).

Since 1992, Greece has been a popular destination for a large number of immigrants from the neighbouring country of Albania. However, these moving populations are characterized by a high prevalence of the viral hepatitis’ serological markers, especially the ones of Hepatitis B (6–9). Moreover, it is believed that there is a declining trend regarding the prevalence of Hepatitis B in Greece among the young population (individuals up to their mid-20s). The HBsAg positivity rate in these age groups is expected to be lower than 1%, whereas the overall anti-HBc prevalence is suggested to be lower than 2% among the same ages (10–12). Therefore, specific public health measures, concerning the surveillance of viral hepatitis in the Albania-deriving populations, have to be induced.

The aim of the present study was to assess the epidemiology of the serological markers of viral Hepatitis B and C among young people from Albania. The findings may allow the authorities to estimate the transmission risk of HBV and HCV, evaluate the present and future consequences for the public health and plan protective and preventive health control measures for the entire population. The target group was focused on people of a certain generation given the fact that there is insufficient published data on the epidemiological trends of Hepatitis B and C among people of this specific age.

Methods

Study population

The present study was conducted in the Regional Medical Department of Pogoniani. The latter is a town located in the prefecture of Ioannina, in north-western Greece, only 12 km from the Greek–Albanian border. Although Pogoniani is a small town, it is a place of settlement for a large number of young immigrants from Albania. The purpose of the presence of these populations is to participate in a series of educational and technical professional courses, which are offered to them by two institutes located in the town. The mean duration of stay in Pogoniani for every immigrant of that kind is approximately two-to-three years. Afterwards, they move to larger cities mainly in Greece and Italy for occupational reasons.

The research was focused on these juvenile immigrants who have recently come from all over the country of Albania, have settled in Pogoniani of Ioannina and participated voluntarily in vaccination programs against Hepatitis B from 2000 through 2009. It is worthwhile to mention that the response rate for these vaccination programmes was 100%, meaning that all immigrants of the specific population accepted the screening examination. Table I shows the distribution of subjects according to year of participation and sex. The study population included a total of 504 subjects, 418 males and 86 females, aged between 10 and 23 years old (mean age ± SD = 15.6 ± 1.4) at the time of examination. There were no exclusion criteria, but any individual patient could only be included once. All the subjects were screened almost immediately after their arrival in Pogoniani from Albania. All the necessary information about their age and sex was obtained from the medical records of the Medical Department of Pogoniani.

Table I. Distribution of subjects according to year 1 of participation and sex.

Year	2000	2001	2002	2003	2004	2005	2006	2007	2008	2009	2000–2009
Males	27	36	40	76	110	19	18	19	40	33	418
Females	5	1	4	14	16	8	12	15	4	7	86
Total	32	37	44	90	126	27	30	34	44	40	504

Data

The study used the results from the tests that were conducted for the ascertainment of the serological status of each participant prior to the immunization against HBV. Each person was subjected to a venesection and the received serum samples were separated by centrifugation, coded and stored at −20°C. Afterwards, each sample was assayed for the Hepatitis B surface antigen (HBsAg), the antibodies against HBsAg (anti-HBs), the total Hepatitis B core antibodies (anti-HBc) and the antibodies against HCV (anti-HCV). Serum samples that were found as HBsAg positive were further tested to detect the possible presence of the Hepatitis B ‘envelope’ antigen (HBeAg), the corresponding antibodies (anti-HBe) and the IgM anti-HBc. All of the above tests were conducted in the Department of Blood Donation of the ‘G. Hatzikosta’ General Hospital of Ioannina with enzyme immunoassays techniques and the use of the ordinary equipment and procedures of the daily laboratory practice.

Analysis

The system Microsoft Excel 2003 (Copyright © Microsoft Corporation 1985–2001) was used for data entry. A χ²-test, performed with the use of the statistical package SPSS 14.0 (Copyright © 2005 SPSS Inc.), was used to detect any differences in the seroprevalence between the two sexes. A P-value of <0.05 was considered as statistically significant.

Results

Of the total 504 subjects, 59 (11.7%) were HBsAg positive, 144 (28.6%) were both anti-HBc and anti-HBs positive, 33 (6.5%) were only anti-HBs positive and (0.2%) was only anti-HBc positive. The overall anti-HBc positivity was 40.5% (204 out of 504), while 267 individuals (53.0%) presented no positive serological marker.

Table II shows the distribution of Hepatitis B serological markers among the study population according to sex. Although the carrier rate of HBsAg was higher in males than in females (12.7% and 7.0%, respectively), the difference was not statistically significant (P > 0.05). However, the overall prevalence of anti-HBc was also higher in males than in females (43.3% and 26.8%, respectively) and this difference was confirmed statistically (P <0.05).

Table II. Distribution of Hepatitis B serological markers according to sex.

	Males		Females		Total
	n	(%)	n	(%)	n	(%)
No serological marker	211	50.5	56	65.1	267	53.0
HBsAg positive (also anti-HBc positive)	53	12.7	6	7.0	59	11.7
Both anti-HBc and anti-HBs positive	128	30.6	16	18.6	144	28.6
Anti-HBs positive alone	26	6.2	7	8.1	33	6.5
Anti-HBc positive alone	–		1	1.2	1	0.2
Total	418	100	86	100	504	100

HBsAg, Hepatitis B surface antigen; anti-HBs, Hepatitis B surface antibody; anti-HBc, Total Hepatitis B core antibody.

Of the 59 HBsAg positive subjects, 5 individuals (8.5%) were identified as HBeAg positive, 3 (5.1%) were both HBeAg and anti-HBe negative and the rest 51 (86.4%) were found as HBeAg negative. Additionally, among the same group, 3 individuals (5.1%) presented positive IgM anti-HBc.

Finally, only 3 individuals (0.6%) presented antibodies against HCV. All of them were males and were anti-HBc and anti-HBs positive.

Discussion

Main results

In areas of high endemicity the most common way of the HBV spread is the perinatal transmission and the infection during the pre-school age, whereas in areas with low endemicity the horizontal transmission is more frequent (13). In the present study, the prevalence of Hepatitis B and C serological markers among juvenile immigrants from Albania was evaluated. We found a high prevalence of all the relative serological markers of Hepatitis B among the study population. The presence of anti-HBc in 204 subjects (40.5%) confirms the endemic nature of HBV infection in the Albanian community. The prevalence of HBsAg was very high (11.7%), particularly in males (12.7%). The percentage of the anti-HCV positive serum samples was very low (0.6%).

Prevalence of Hepatitis B

The high prevalence figures of HBsAg are comparable to the rates observed in countries with high endemicity of HBV, such as parts of China, Southeast Asia, tropical and sub-Saharan Africa and Middle East (14). Our results are confirmed by a study recently conducted inside the country of Albania, which demonstrated a high prevalence of the HBV infection among the Albanian population, especially in the younger age groups, such as in schoolchildren, and in military personnel (HBsAg prevalence equal to 11.8% and 10.6%, respectively) (15).

Transmission of Hepatitis B

By studying the specific sample, we can draw valuable conclusions about the potential risks for the general population. There are no large comparable studies, regarding people of this specific age group from Albania, which have been recently done in southern Europe, where the problem is primarily focused. Epidemiological studies carried out in different parts of the world show that the characteristics of the population, such as socio-economical factors, sanitary conditions, lifestyle and hygiene are related to large variations in the frequency and prevalence of HBV and HCV infection. Subsequently, due to potential different social circumstances and habits the immigrants can constitute a special social group in the community, which influences viral hepatitis’ prevalence in a geographic area. Their epidemiological impact depends on the endemicity of viral hepatitis in their country of origin.

The specific age range of the study population indicates that HBV infection was acquired early in life, either from mother-newborn transmission or from household and other non sexual horizontal contacts. The perinatal transmission of HBV may occur either if the mother is a chronic HBsAg carrier or if she has an acute HBV infection. The presence of maternal HBeAg increases the risk of perinatal transmission of HBV to the neonate. In fact, the risk of transmission is 70–90% in newborns from HBeAg positive mothers, whereas the respective risk from mothers who are both HBsAg positive and HBeAg negative is 10–40% (16). Indeed, there is published evidence indicating the high prevalence of HBsAg and HBeAg among pregnant women from Albania (17).

The presence of HBeAg indicates active viral replication, high viral load and increased infectivity (18). There were 3 chronic HBsAg carriers who were both HBeAg and anti-HBe negative. These subjects were possibly carriers of a variant strain with a pre-core mutation that prevents the HBeAg production (19).

The IgM anti-HBc indicates an acute HBV infection and can be used for differentiation from a chronic infection (20). In our study population, the great majority (94.9%) of the HBsAg carriers were chronically infected by HBV, since they did not present positive IgM anti-HBc.

The likelihood of developing chronic HBV infection is higher in individuals who are infected perinatally (90%) or during childhood (20–30%), when the immune system is thought to be immature, compared with immunocompetent subjects infected during adulthood (<1%) (21).

Implications

The potential complications of chronic viral hepatitis are very important and include cirrhosis, hepatic decompensation, hepatocellular carcinoma and extra-hepatic diseases (polyarteritis nodosa, membranous glomerulonephritis and leukocytoclastic vasculitis) (22). An increasing immigrating population with a high prevalence of Hepatitis B can influence the epidemiologic trends of the indigenous population in southern Europe. The immigrants become a part of the community as time goes by and can affect the epidemiology of viral hepatitis and its complications of the general population (23–26). The problem becomes more serious, if we take into account that this particular group of subjects are young and thus, their life expectancy allows the chronological progression of the entire chronic liver disease's sequence.

Measures

Because of the seriousness of the problem, certain policies against the spread of HBV in the community have to be introduced. The authorities should establish public health programs that aim at the surveillance, prevention and control of viral hepatitis. Active detection of the HBV infection in specific regions and populations with the appropriate serologic tests is necessary. Additionally, a series of educational campaigns, which provide information about viral hepatitis, should be organized for both the general population and the immigrants. The chronic carriers of HBV should be advised to follow a life-long medical monitoring and adapt their lifestyle to protect their health condition and prevent the transmission of HBV to others (27). Moreover, the health authorities could contribute to the immunization of the sensitive immigrating population by providing the necessary resources.

Conclusion

In accordance with other studies, the results of the present study demonstrate a high prevalence of the Hepatitis B serological markers among the specific Albanian migratory population. Thus, specific public health measures are necessary. The low percentage of anti-HCV positive serum samples indicates no potential public health dangers regarding Hepatitis C.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.