Abstract

Background: Increased migration volume and different Hepatitis B prevalence between immigration and emigration countries have changed the Hepatitis B virus (HBV) epidemiology considerably in Northern and North-Western European migrants-receiving countries. Due to the difference in migration status monitoring, the HBV infection data on migrants are not easily comparable among those countries. The study aims were: to compare the migration status indicators used by the national surveillance system in six Northern and North-Western European countries (the Netherlands, Germany, Finland, Denmark, Sweden and the UK); to determine the impact of the migration status on HBV infection by comparing the available data on prevalence and transmission routes of Hepatitis B in the migration and the general population in the six countries; to recommend sensible indicators and pertinent measures for HBV infection surveillance and control in the region. Methods: Literature review, statistical data analysis on migration and HBV infection in the six countries; expert interviews to identify migration status indicators used in national surveillance systems. Results: Evident differences were found between the migration and the general population in Hepatitis B prevalence and transmission routes in the six countries. Migration status is monitored differently in six surveillance systems; immigrants from high/intermediate Hepatitis B endemic countries constitute a substantial proportion of HBsAg+ and chronic cases in all six countries. Conclusions: International migration has an obvious impact on Hepatitis B prevalence in the six countries. It is important to include common migration status indicators and to collect comparable data for HBV infection surveillance in different notification systems.

Introduction

The fact that ethnic composition of the European population is changing has major influence on the demands for health-care sectors. In Northern and North-Western Europe, the national incidence of infectious diseases such as Hepatitis B virus (HBV) infection, was reduced to very low levels, this is far in advance than in the other parts of the world.1 In recent years, mostly due to the increased migration from countries with intermediate/high HBV prevalence, HBV infection has again become a public health concern in Northern and North-Western Europe. Migrants crossing the prevalence gaps have become the majority of case load in low incidence migrant receiving countries.2 Based on reported cases, incidence rates of Hepatitis B decreased across Europe due to vaccination, changes in risk behaviours and prevention programmes, but the figures reflect in most of the cases, only acute Hepatitis B infections. The prevalence of chronic Hepatitis B and HBV carriers is actually constant or even increasing mostly due to migration; this fact is not apparent due to a lack of relevant data.3 The first surveillance report of the European Centre for Disease Prevention and Control (ECDC) (2007) found significant heterogeneity in the availability and quality of data on Hepatitis B across Europe. It is essential to develop reliable and comparable data collection systems that measure the full burden posed by HBV in Europe, so that appropriate measures can be taken to reduce this burden.4 The study aims were to compare the migration status monitoring in six Northern and North-Western European countries (the Netherlands, Germany, Finland, Denmark, Sweden and the UK), to determine the impact of the migration on HBV infection by comparing the available data on prevalence and transmission routes of HBV in the migration population and the general population in those countries, and to recommend sensible indicators and pertinent measures for HBV infection surveillance and control in the region.

Methods

Country and data selection

To establish an impression of the migration impact on HBV infection and surveillance, we focused on Northern and North-Western Europe where the import of HBV infection through migrants plays an important role for the epidemic. Data on notified HBV infection and Hepatitis B surveillance were collected from the websites of ECDC, World Health Organization (WHO) and six national surveillance systems: RIVM—National Institute for Public Health and the Environment (the Netherlands), RKI—Robert Koch-Institut (Germany), KTL—National Public Health Institute (Finland), SSI—The Statens Serum Institute (Denmark), SMI—The Swedish Institute for Infectious Disease Control and HPA—Health Protection Agency (the UK). Migration status data were obtained from the websites of the corresponding national statistics authorities, Focus-migration and European Migration Network.

Literature review

To summarize the epidemiology of Hepatitis B in the six countries, a literature review was performed. Articles indexed in the PubMed database, which were published from January 1990 to February 2009 in English or German language or with an English abstract available, were searched by using the following key words: Hepatitis B and migrants/immigrants, incidence, prevalence and names of the investigated countries. Further literature was identified by the snowball method.

Additional information by national experts

In the case of the Netherlands, Finland, Germany and Denmark, in which migration status indicators used by the surveillance systems could not be identified by literature, experts of the corresponding national authorities were interviewed through e-mails. The following questions were included in the letter: are data on the ethnic background, social–economic status collected in the national surveillance system? Can the Hepatitis B surveillance data be linked to general statistics and what is the estimate about under-reporting of Hepatitis B infection in the country?

Data analysis

Based on the collected data on HBV infection and migration status, a descriptive data analysis was made; migration status, Hepatitis B epidemiology and HBV infection in migrants in the six countries was reported and compared.

Results

The Netherlands

Migration status

The Dutch government distinguishes between ‘allochtonen’ and ‘autochtonen’, Allochtoon is the manufactured opposite of the Greek term autochthon, which means ‘native’. Allochtonen are persons who were born outside the Netherlands or who have at least one parent who was born outside the Netherlands. Western and non-Western allochtonen are also distinguished, non-Western allochtonen are defined as people from Turkey, Africa, Latin America and Asia (excluding Indonesia and Japan). Of the total population, 19.3% (2006) is allochtoon (10.6% non-Western), 9.8% is foreign born; 39% of non-Western allochtonen live in the four largest cities, as compared with 13% of the Dutch population.5 In recent years, there has been a significant immigration decrease in the Netherlands, which might have an impact on future epidemic trends.6

HBV epidemiology

The estimated overall prevalence of HBsAg in first-generation migrants (FGMs) was 3.77% (0.32–0.51% in the Dutch population), 70% of the chronic Hepatitis B patients were born abroad (2006).7 The estimated prevalence of HBsAg in large cities was three to five times higher than in rural areas.8 Among acute cases, sexual contact was the most important risk factor (65% in 2007), with an equal proportion of men who have sex with men (MSM) and heterosexual contact; infection due to injection drug use (IDU) (0.9%) was low. A difference in HBV transmission route between Dutch and immigrant populations was noted. In the Dutch population, sexual transmission accounted for the largest proportion of infections, whereas perinatal transmission was reported to be higher in non-Dutch population. Imported HBV infections had small impact on MSM (who were mostly of Dutch origin), but determined the prevalence among the heterosexually infected persons.7

Germany

Migration status

In Germany, the term ‘persons with a migration background’ refers to persons who have either immigrated themselves or are the second- or third-generation descendants of immigrants. Of the total German population, 19% is with a migration background (2005). Among them, 5.6 million are with personal migration experience, 3 million are naturalized citizens and 1.8 million are re-settlers (ethnic Germans from Eastern Europe and the former Soviet states).5 In the earlier 1990s, more than 1 million immigrants entered Germany annually (among them, numerous re-settlers). In the last decade, Germany had a declining immigration trend.6

HBV epidemiology

Of the adult migrant population in Germany, 84% migrated from intermediate/high HBV prevalence countries. The risk for HBsAg+ was 7.1 times higher for re-settlers and 4.3 times higher for foreign citizens than for the German population, people with a migration background accounted for 42% of HBV carriers in Germany (2003).9 Among acute HBV infections (2002), common transmission routes were heterosexual contacts (42%), IDU (16%) and homosexual contacts (6%). The prevalence of anti-HBc was higher in Western German states than in Eastern, the city with the highest proportion of foreign residents had also the highest Hepatitis B incidence rate.10 For children and adolescents, the prevalence of anti-HBc in first-generation migrants was 15 times higher and in second-generation migrants, 3 times higher than in non-migrants; the anti-HBc prevalence was significantly higher among children from families with low socio-economic status than those from families with high socio-economic status (2006).11 The number of notified Hepatitis B cases has been decreasing since 1997.3

Finland

Migration status

From 1990 to 2009, the number of foreign citizens legally residing in Finland increased 6-fold. Of the Finnish population (2009), 5% claims a foreign background (foreign born, foreign citizenship or foreign language as mother tongue).12 Citizens from Russia and Estonia form the two largest migration groups in Finland. Many of these two groups are re-settlers of Finnish origin. More than 20 000 refugees live in Finland. The immigrant population is heavily concentrated in Southern Finland, especially in the ‘metropolitan’ area of Helsinki.13

HBV epidemiology

In the late 1990s, Finland experienced nationwide HBV infection outbreaks among drug users and their sex partners.14 In 2006, 37 acute Hepatitis B cases were notified in Finland, which was slightly more than one-tenth of the top figure in 1997. The majority of cases (19) was diagnosed in the Helsinki and Uusimaa hospital districts.15 Among 17 acute cases, the transmission routes were identified (2008), 13 had been contracted through sexual contact, 2 through IDU.15,16 In recent years, the majority of notified carriers and chronic Hepatitis B cases was of foreign origin, practically all infected neonates in Finland are foreigners.15

Denmark

Migration status

In Denmark, an immigrant is defined as a person born abroad whose parents both are foreign citizens or were born abroad. A descendant is defined as a person born in Denmark whose parents are either immigrants, or descendants with foreign citizenship. Immigrants and their descendants constituted 8.4% of the Danish population (immigrants 76%, descendants 24%) (2005), 71% of them are from a non-Western country.17 More than half the growth of the Danish population in the last 35 years can be accounted for by immigrants and their descendants. Most ethnic groups in Denmark are rather small, 25% of all foreigners in Denmark belong to groups that are each smaller than 1.5%.18

HBV epidemiology

Over the past 20 years, the prevalence of HBsAg carriers in the indigenous population has declined from 0.15% to 0.03%; but the overall number of HBsAg carriers in Denmark has not changed due to the increased number of immigrants from high endemic areas.19 Based on SSI-traced chronic Hepatitis B infection in 2000–04, 72% was mother-to-child transmission, and 99% of these cases were from immigrant children. During 2000–03, IDU was the most common mode of transmission for Danish-born people; since 2004, heterosexual transmission was the most common transmission route.20

Sweden

Migration status

In Sweden, the term ‘person of foreign background’ refers to Swedish citizen, either foreign born or Swedish born with both parents foreign born; foreign citizenship or asylum seekers. In 2007, people of a foreign background, foreign born and foreign citizens were 17.3, 13.4 and 5.7% respectively, of the total population and 0.39% of all persons with a foreign background were asylum seekers.21 Mainly due to family reunifications the immigration has increased in recent years in Sweden.6

HBV epidemiology

Based on a study (1995–96), among acute HBV infections, the probable transmission routes were IDU (46%), heterosexual contact (25%); transmission from immigrants was of minor importance.22 Among chronic HBV infections, 87.7% of notified cases were of foreign origin (2001).23 Since 2007 there has been a slight increase in the number of both acute and chronic Hepatitis B cases in Sweden; among 1514 cases notified in 2008, 13% were acute infections, most chronic carriers were members of immigrant families from endemic areas.24

The UK

Migration status

Although immigrants are often popularly thought of as minority ethnic populations in the UK, for statistical purposes, they are more narrowly described as current residents born outside of the UK. Of the total population (2001) of the UK, 8.3% was born overseas.5 The largest immigrant increase in the post-war decades occurred in the decade from 1991 to 2001. In 2004–07, UK had the unexpected large inflows of A8 nationals (nationals of the Czech Republic, Estonia, Hungary, Latvia, Lithuania, Poland, Slovakia and Slovenia), yearly net immigrants were three times of that of the early 1990s.6

HBV epidemiology

Estimates assume that the Hepatitis B incidence in England and Wales is 5.5–7.4/100 000/year (1995–2000); this figure cannot distinguish between acute and chronic infections.25 For acute infections, IDU was the most frequently reported route of transmission, but it becomes clear that sexual transmission is the principal identified route of transmission since it seems likely that many of the ‘No identified risk’ cases were acquired sexually.26 Chronic infections in migrants were estimated to account for 96% of all chronic Hepatitis B infections newly added to the existing number of such infections in England and Wales (1995–2000).27 The majority (122 000 cases) of estimated Hepatitis B carriers in the UK (150 000–200 000 cases) live in London, whereas half of the UK ethnic minorities constitute one-third of the London population.28 Since 2006 there has been a small increase of confirmed acute Hepatitis B cases in England and Wales.26

Comparison of the six countries

Incidence and prevalence

In all six countries, the incidence of notified HBV infection in the total population is decreasing (figure 1).29 The prevalence of HBsAg in the base population is different in the six countries (0.01–0.7%),30 but the prevalence of HBsAg in three largest migrant groups in all six countries is similar: ∼4% (4.6% in Finland) (table 1).31

Figure 1

Hepatitis B incidence per 100 000 populations per year in six Northern and North-Western European countries based on data of the WHO (2007)

Figure 1

Hepatitis B incidence per 100 000 populations per year in six Northern and North-Western European countries based on data of the WHO (2007)

Table 1

Migration status and HBV infection

 The Netherlands Germany Finland Denmark Sweden UK 
Foreign born/non-citizens in total population (%), 200332 10.1/4.2 12.5/8.9 2.5/1.7 6.8/5.0 12.0/5.3 8.3/4.5 
Percent of three largest migrant groups in foreign born 2001–036 Turkey 11.1, Suriname 11.0, Morocco 9.5 Turkey 26.1, Italy 8.3, Former Yugoslavia 8.1 Russia 23.9, Sweden 18.8, Estonia 6.2 Turkey 9.3, Germany 6.8, Iraq 6.0 Finland 18.8, Former Yugoslavia 7.1, Iraq 5.4 Ireland 10.9, India 9.6, Pakistan 6.6 
HBsAg+ in three largest migrant groups (%) (2010)31 4.0 4.0 4.6 4.0 4.0 4.0 
HBsAg+ in general population (%) 2005–0730 0.3 0.7 0.23 0.01 0.03 0.3 
Under-reporting estimate (%) 6033 803,4 No info 5030 No info 2530 
Immigrant indicator/link to population statistica Country of birth of the infected and the mother/No No/No Country of birth/Yes Migrant or country of origin/Yes Country of birth/Yes Ethnic group (acute HBV)/No 
 The Netherlands Germany Finland Denmark Sweden UK 
Foreign born/non-citizens in total population (%), 200332 10.1/4.2 12.5/8.9 2.5/1.7 6.8/5.0 12.0/5.3 8.3/4.5 
Percent of three largest migrant groups in foreign born 2001–036 Turkey 11.1, Suriname 11.0, Morocco 9.5 Turkey 26.1, Italy 8.3, Former Yugoslavia 8.1 Russia 23.9, Sweden 18.8, Estonia 6.2 Turkey 9.3, Germany 6.8, Iraq 6.0 Finland 18.8, Former Yugoslavia 7.1, Iraq 5.4 Ireland 10.9, India 9.6, Pakistan 6.6 
HBsAg+ in three largest migrant groups (%) (2010)31 4.0 4.0 4.6 4.0 4.0 4.0 
HBsAg+ in general population (%) 2005–0730 0.3 0.7 0.23 0.01 0.03 0.3 
Under-reporting estimate (%) 6033 803,4 No info 5030 No info 2530 
Immigrant indicator/link to population statistica Country of birth of the infected and the mother/No No/No Country of birth/Yes Migrant or country of origin/Yes Country of birth/Yes Ethnic group (acute HBV)/No 

a: Source: European Centre for Disease Prevention and Control30 and expert interview.

Notification, vaccination and screening programmes

‘Country of birth’ of the infected person is collected by the national surveillance systems as migration status indicator, except in Germany and the UK (table 1). Notifiable for Hepatitis B infections are mainly lab-confirmed, acute and chronic cases (Germany, only acute), Sweden includes also probable cases, the UK includes asymptomatic.

Germany practices a general vaccination of all newborns plus risk group strategy since 1995, the Netherlands has started universal Hepatitis B vaccination since October 2011, the other investigated countries practice risk group vaccination policy as Sweden currently reviews plans for introducing universal Hepatitis B vaccination in the near future. Each country has its vaccination and screening programmes for risk groups (table 2). In all six countries, neonates born to HBsAg+ mothers, individuals at risk for HBV due to occupation, IDUs and household contacts of HBsAg+ patients are recommended for vaccination; pregnant women, blood and organ donors are recommended for screening.30

Table 2

Vaccination groups and screening programmes30

  The Netherlands Germany Finland Denmark Sweden UK 
Vaccination groups Neonates born to HBsAg+ mothers Yes Yes Yes Yes Yes Yes 
Individuals at risk for HBV due to occupation Yes Yes Yes Yes Yes Yes 
Injecting drug users Yes Yes Yes Yes Yes Yes 
Household contacts of HBsAg+ patients Yes Yes Yes Yes Yes Yes 
Haemodialysis patients Yes Yes No Yes Yes Yes 
STI clinic patients No Yes No No No Yes 
Contacts of infected persons No Yes No Yes Yes Yes 
Chronic liver disease patients No Yes No Yes No Yes 
Multiple sex partners Yes Yes No No Yes Yes 
Others Yes Yes Yes Yes No Yes 
Screening programmes Pregnant women Yes Yes Yes Yes Yes Yes 
Blood and organ donors Yes Yes Yes Yes Yes Yes 
Injecting drug users No Yes No Yes Yes No 
STI clinic patients No Yes No No No No 
Multiple sex partners No Yes No No No No 
Prisoners No Yes No No Yes No 
Haemodialysis patients No Yes No No Yes Yes 
Health-care workers No Yes No No No No 
Workers who are occupationally exposed to the virus No Yes No No Yes Yes 
  The Netherlands Germany Finland Denmark Sweden UK 
Vaccination groups Neonates born to HBsAg+ mothers Yes Yes Yes Yes Yes Yes 
Individuals at risk for HBV due to occupation Yes Yes Yes Yes Yes Yes 
Injecting drug users Yes Yes Yes Yes Yes Yes 
Household contacts of HBsAg+ patients Yes Yes Yes Yes Yes Yes 
Haemodialysis patients Yes Yes No Yes Yes Yes 
STI clinic patients No Yes No No No Yes 
Contacts of infected persons No Yes No Yes Yes Yes 
Chronic liver disease patients No Yes No Yes No Yes 
Multiple sex partners Yes Yes No No Yes Yes 
Others Yes Yes Yes Yes No Yes 
Screening programmes Pregnant women Yes Yes Yes Yes Yes Yes 
Blood and organ donors Yes Yes Yes Yes Yes Yes 
Injecting drug users No Yes No Yes Yes No 
STI clinic patients No Yes No No No No 
Multiple sex partners No Yes No No No No 
Prisoners No Yes No No Yes No 
Haemodialysis patients No Yes No No Yes Yes 
Health-care workers No Yes No No No No 
Workers who are occupationally exposed to the virus No Yes No No Yes Yes 

STI, Sexually transmitted infection.

Discussion

Even though we included only six Northern and North-Western European countries, it becomes obvious that the surveillance data of different countries are not easily comparable; common migration status indicators and comparable data for HBV infection surveillance in different notification systems are of importance. In figure 1, which shows the Hepatitis B incidence rate, Finland does not differentiate chronic and acute cases; the increase (1999–2001) of reported acute HBV cases in the Netherlands was mainly caused by the implementation of adding chronic carriers to the mandatory reporting system in 1999; whereas the sharp decrease in the number of reported cases in Germany resulted mostly from only reporting acute cases since 2001 in the country.29 The numbers of non-citizens and foreign born are quite different (table1), our results show that being foreign born is an important factor for HBV infection but for statistics, normally nationality is used.6 Although the prevalence of HBsAg among German re-settlers, who are registered as German citizens, is much higher than the general population (due to the intermediate/high HBV prevalence in their emigration countries of the former Soviet states), the impact of this migrant group on HBV infection in Germany is not reflected in the national surveillance data, because chronic HBV infections and the country of birth of the infected person are not notifiable in Germany.

Finland seems specifically successful in controlling Hepatitis B infection through needle and syringe programmes (NSPs) and health counselling in the last decade. NSPs are also available in the Netherlands, Germany, Denmark and the UK, but not in Sweden.3,14,28,30 Hepatitis B is increasingly being considered as a sexually transmitted infection (STI).26 But HBV infection is different from other STIs, as most of those are acute infections and their epidemic is not largely driven by migrants in the observed countries. It has become evident that young migrants and children of migrants had been frequently approached by drug dealers; IDU in migrant groups frequently involves more sharing and poor cleaning of equipment than in other groups of similar age and socio-economic background.35 The experience of Denmark, the Netherlands, Sweden and the UK indicated that the selective targeted vaccination programmes are not effective in controlling HBV infection, especially for drug users and people at risk of Hepatitis B infection through sexual contacts.16,26,36,37 In contrast, vaccination of children of immigrants from endemic countries seems to be an effective strategy.38 Due to high under-reporting rates (25–80%) (table 1) and the difficulty in identifying all at-risk individuals, we recommend universal Hepatitis B vaccination for newborns and infants. The benefits of this strategy are: opportunities to combine Hepatitis B vaccination with existing universal vaccination programmes for newborns and infants; impact on perinatal transmission, if vaccination is started shortly after birth; higher impact on chronic carrier rate and transmission even with a delayed impact on sexual transmission of HBV.39

We recommend using ‘person with a migration background’ to refer to immigrants and their descendants for migration status monitoring in Hepatitis B surveillance, since the prevalence of HBsAg and anti-HBc is much higher among the naturalized and the second-generation immigrants than the general population (table 1).11,30,31 The example of A8 national inflow to the UK has made EU-wide uniform case definition and comparable data collection of importance. The connection between the prevalence of anti-HBc and socio-economic status draws attention to adding the related information to surveillance data. Evidently, it is essential to make a link between Hepatitis B surveillance data and the national population registry for determining incidence and prevalence.4

Limitations

Due to under-reporting and the fact that two-third of Hepatitis B infection is asymptomatic, the reported rate considerably underestimates the true incidence of Hepatitis B in the region. Owing to limited data availability, most figures used were from organizational websites and studies published within different years, main HBV infection data for the UK were from England and Wales. Due to language barrier studies and reports that were presented by other European languages, than English and German, could only be used to a limited extend. Even though the authors have tried to close this information gap by interviewing national experts, it is possible that some important reports or data are missing.

Conclusions

This study shows that, despite the very low incidence of Hepatitis B in Northern and North-Western European countries, international migration has an obvious impact on the Hepatitis B prevalence in the investigated countries. Unified data collection with regards to migration status is of importance in different HBV infection surveillance systems.

Funding

This paper is a product of the work package “Infectious diseases” of the project MEHO, Migrant and Ethnic Health Observatory. This project was funded under the framework of Public Health Programme 2003–2008 of the European Commission (contract number 2005122).

Conflicts of interest: None declared.

Key points

  • Confirm heterogeneity in the availability and quality of data on Hepatitis B in Northern and North-Western Europe.

  • Provide evidence of similar impact of the migration status on HBV infection in Northern and North-Western European countries with different immigrant composition and proportion.

  • Show the importance of using uniform data collection and comparable migration status indicators in Hepatitis B surveillance in the region.

Acknowledgements

We thank Mika Salminen (KTL), Femke Koedijk and Maaike van Veen (RIVM), Hermann Claus (RKI), Susan A Cowan (SSI), Pauli Leinikki, Bruce Ullrich, Gaby Zeck, Andrea Kattein, Felix Greiner, Kai Schnackenberg, Dirk Gansefort, Julia Röttger and Gerda Längst for valuable information and support of this project.

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