Background
Hepatitis B is one of the major infectious diseases in the world [
1]. It is a notifiable disease in the Netherlands, and each year around 1,800 hepatitis B virus (HBV) infections are reported nationally, of which 79% are chronic [
2]. Chronic HBV infections cause 23% of all liver cancers in the Netherlands and are an important problem in ethnic minority groups, such as the Turkish community, which is the largest group of immigrants from newly or non-industrialized countries in the Netherlands [
3,
4]. The Turkish immigration in the Netherlands dates back to the sixties, when Dutch industries started to recruit abroad in order to attract extra labour forces. They targeted various countries of the Mediterranean. It was a joint effort of several Western European nations. As a result, between the end of World War II and the mid-seventies, guest workers came to the Netherlands and other North European countries, departing from several countries of the Mediterranean, including Spain, Italy, Morocco and Turkey. What was first meant to be a temporary migration turned into a permanent stay, as many immigrants settled in the Netherlands and later had their families come over for reunification [
5,
6]. While the Turkish community represents 7.7% (45,415 persons) of the total city population in Rotterdam, it accounts for 30% of reported chronic HBV infections [
7‐
9]. Seventy percent of all infections (i.e. acute and chronic infections) in the Turkish-Dutch population involve people aged between 16 and 40. In this group, the mean incidence of reported HBV infections is 122 per 100,000 Turkish-Dutch individuals, much higher than the 35 infections per 100,000 persons reported in the total population of Rotterdam, and the 9 infections per 100,000 persons reported in the general Dutch population [
2]. However, these figures underestimate the population-prevalence, because many chronic hepatitis B patients do not have symptoms of disease and are therefore not reported. Population-based studies indicate a prevalence of chronic HBV infections of 0.2% in the general Dutch population, and a much higher prevalence of 2.6 - 4.8% in the Turkish-Dutch population [
4,
8,
10,
11].
Transmission in migrant populations (such as Turkish migrants) in low-endemic countries (such as the Netherlands) likely reflects the transmission pattern of the country of origin; most individuals in the Turkish community have acquired HBV through vertical transmission (from mother to child during birth) [
2]. However, in (young) adults the most important route of transmission is through horizontal transmission (i.e. sexual contact) [
12]. A study in the Netherlands demonstrated that in 60% of the heterosexual cases of hepatitis B, the source of infection was a partner originating from an HBV-endemic region [
13]. As 75-80% of the married Turks in the Netherlands are married to someone from Turkey (marriage migration) [
14], the risk of horizontal transmission in the Turkish community is still high. It is estimated that immunization of persons with partners of non-Dutch nationality could prevent 36% of hepatitis B cases in heterosexuals [
15].
Control of HBV infection presently focuses on screening pregnant women and vaccinating specific risk groups, such as newborns, children with a parent from an HBV endemic area (such as Turkey), and people with high-risk sexual behaviour [
12]. Although these programmes are well-attended, there is no specific strategy for the detection and prevention of HBV in the adult Turkish-Dutch population. Screening for HBV should therefore be promoted in this group through public health interventions, in order to detect individuals eligible for treatment and to prevent horizontal transmission in sexually active and pre-active individuals. To develop these interventions, determinants of screening behaviour need to be identified. Studies of migrant groups in the USA have identified several behavioural factors that influence participation in HBV screening. These include the level of knowledge, attitude towards screening, perceived severity, perceived susceptibility, self-efficacy, cultural beliefs (e.g. traditional medicine), accessibility of health care, and demographic factors such as age, education, language proficiency, length of stay in the new country, having health insurance, and socio-economic status [
16‐
25]. Studies into preventive behaviour (e.g. breast cancer screening) of Turks in either Turkey or the Netherlands report relevant determinants such as educational level, knowledge/former education about the disease, confidence, perceived susceptibility, seriousness, barriers and benefits [
26‐
33]. Literature on the access of migrants to the Dutch health care system suggests that the most important barrier is communication between health care providers and clients [
34]. Barriers in access and stigma have been reported by migrant black Africans with regard to HIV testing [
35], but not with regard to HBV testing. Health insurance is obligatory in the Netherlands, and most health care costs will be re-imbursed by this insurance. However, this is often not the case for self-initiated hepatitis B testing and vaccination of adult migrants, as they are not formally defined as a risk group by the Ministry of Health. Therefore, the costs incurred might be a barrier for testing and vaccination in Turkish Dutch.
When health education places a strong emphasis on individual cognitive processes, and pays limited attention to the embeddedness of human health behaviour in cultural contexts and social structures, this may lead to low effectiveness of interventions. Therefore, basing interventions not just on behavioural constructs but also on socio-cultural factors, is expected to enhance the reception and appreciation by the public [
36,
37]. Anthropological and migrant studies revealed some plausible relevant socio-cultural determinants related to HBV screening [
38‐
43]. These are social influences such as social norms and social support, and cultural aspects such as the sensitivity regarding sexuality, the importance of reputation, and responsiveness to authority. Also, as the majority of the Turkish-Dutch population is Muslim, religion may be an important determinant of screening through its doctrine regarding health and disease, religious responsibility, the concept of cleanliness, and of what is considered (un)lawful ('haram/halal'). To our knowledge, socio-cultural factors influencing the HBV-screening behaviour in the Turkish-Dutch population have not been investigated.
The aim of this study was to investigate behavioural and socio-cultural determinants associated with hepatitis B screening in the Turkish population in the Netherlands, in order to develop culturally appropriate interventions. The study applied a combination of qualitative and quantitative research methods, by means of focus group discussions and a survey. This paper reports the findings from the qualitative study, which aimed to obtain insight into socio-cultural determinants and underlying mechanisms that influence the enrolment in HBV-screening by the Turkish-Dutch population. Furthermore, we explored the relevance of these determinants in four subgroups distinguished by gender and migrant generation.
Results
Demographics
In total, seven focus group discussions were held. Age and generation of the participants are presented in Table
1. All parents of the 54 participants were born in Turkey. The majority of G2 participants were not married (82%) and did not have children (91%). G1 participants in most cases were married (78%) or widowed/divorced (6%) with children. Of the participants with children, 45% had children aged 16 and above (sometimes in combination with younger children). The majority of men (74%) reported to have a medium level education, two had university level education and four attended primary school only. Two women had not received any education and 32% attended only primary school, while the majority had a medium (45%) or higher (16%) level of education. The participants were asked to score their Dutch language proficiency (level 1-3/poor-excellent); the mean score for men was 2.14 while this was 2.06 for women. The groups from the disadvantaged suburb did not differ from the other groups regarding level of education and Dutch language proficiency. Most of the G1 participants were older compared to those in the G2 groups. To increase readability, we will sometimes use the terms 'older women' or 'older men' when reporting on G1 participants. For G2 participants we will sometimes use the terms 'young(er) men', 'young(er) women', 'boys' or 'girls'.
Table 1
Composition of the Focus Group Discussions regarding age and migrant generation
Women | | | | | | | |
group G1A | 7 | 19 | 43 | 33.3 | 5 | 1 | 1 |
group G1B | 8 | 26 | 69 | 44.8 | 0 | 7 | 1 |
group G2 | 8 | 17 | 22 | 20.0 | 2 | 0 | 6 |
low SES group4
| 8 | 25 | 47 | 32.9 | 5 | 2 | 1 |
Total | 31 | | | | 12 | 10 | 9 |
Men | | | | | | | |
group G1A | 9 | 36 | 76 | 46.2 | 4 | 4 | 1 |
group G1B | - | - | - | - | - | - | - |
group G2 | 5 | 17 | 19 | 18.2 | 0 | 0 | 5 |
low SES group4
| 9 | 18 | 24 | 19.8 | 2 | 0 | 7 |
Total | 23 | | | | 6 | 4 | 13 |
Social factors
Determinants in the social realm that influence the screening and/or vaccination behaviour may be (1) the social perception of hepatitis B, (2) the social norm regarding screening, (3) the social norm regarding vaccination, and (4) the social support regarding HBV screening.
Regarding the social perception of hepatitis B, initially none of the groups expressed a negative feeling. G1 women mentioned:
"Hepatitis B is a subject that everyone has to deal with. It has to do with health, and how to control one's health. It's not something that affects one's honour".
Only when during the discussion it became clearer that HBV infection might be caused by sexual contact, the subject became more sensitive. The older women discussed the possibility of people talking negatively about them. In addition, the girls started thinking about sexual contact as a mode of transmission and became less confident about the acceptability of the disease. In most groups, it was expressed that there is little knowledge about the sexual mode of HBV transmission, and that this ignorance does prevent that people with hepatitis B are stigmatised. Illustratively, a participant in the G1 men expressed:
"People just do not know much about this disease. They simply come for a sick-call at home, and do not bother about it".
If the level of knowledge would increase, and it would become commonly known that HBV is a sexually transmitted disease, this might lead to social stigma. In contrast, the women from the disadvantaged area mentioned that everyone should be educated so there would be less social stigma surrounding HBV. G1 men and women compared the stigma surrounding AIDS and HBV, and expressed that HBV is perceived totally differently. They felt it was impossible to discuss AIDS with the wider social environment, while HBV was well discussable. The young men in the disadvantaged area, however, did initially associate HBV with AIDS, as "you get it in the same way as AIDS".
As for the social norm regarding screening, there were generally no objections to having a blood test. In fact, having a medical check-up (including broad-spectrum blood tests) when visiting Turkey seemed to be common practice, especially in the aging population. G2 men (and less strongly, G2 women) noted that it might be inefficient to have too many blood tests. The G2 men expressed:
"Well, you might not want to go for a test, because you just intend to live a healthy life. I am not doing a test, just like that. I will first have a look at myself: where did I go wrong, and primarily I will correct myself in that (risk) behaviour".
It was also noted that the G1 women resisted social norms whether or not people should have a HBV-test, illustrated by the following quote:
"As long as I am confident about myself, the others are not important. If we constantly have to think about what others will say about us, we could not do anything with our lives! People will always talk. The more openly you discuss things, the less gossip there will be". (G1 women)
Thus, while the existence and influence of social norms was acknowledged, it was also seen as something that should be fought. Men seemed to perceive little social influence, which became clear from expressions such as: "What other people think, does not affect me".
When the social norm regarding vaccination was discussed, all groups had difficulties finding reasons to object to vaccination.
"If there is a good vaccination for this disease, that is the best action to take!" (G1 women)
Vaccination was perceived as a positive action, and many even expressed the intention to get vaccinated and stimulate others to do the same.
Social support regarding HBV screening was extensively discussed by G1 women who spoke of themselves as supportive mothers, and to a lesser extent, supportive wives. The bond with their children was important; they gave the impression that they would support their children even though they might have contracted HBV by sexual contact (which is disapproved of).
"I will ask them (the children) why they want to go for screening. I will just ask, not because I do not trust what they have done. Whatever has happened, if there is a risk for having contracted a disease, of course they should go for a test." (G1 female participant)
In a less obvious way, this seemed also to be true for supporting their husband; if he planned to be screened this would be encouraged, but not without asking an explanation of the reason why he wanted to be tested. For themselves, the G1 women did not speak about support from their husbands or children. They seemed to be making independent choices about health screening, with a husband who was either indifferent or (distantly) supportive. The G2 women expressed that in general health issues, there was a lot of social support in Turkish families: in going for treatment, in being compliant with treatment, and by giving psychological support when ill. However, regarding the social support for HBV-screening we could distinguish three different opinions in the G2 women groups. First, some girls seemed to have an open relationship with their parents.
"I can discuss anything with my parents, because they will always support me." (G2 women)
Second, some girls considered a test for a sexually transmitted disease (STD) as a private matter, which they would not like to discuss with their parents. Should they really be ill, then they would expect the family to be supportive. Third, there were girls who perceived HBV infection mainly as an STD and strongly felt their parents' rejection of (extra- or pre-marital) sexual contacts. Although they might be supported in the end, the barrier for sharing this with their parents was very high and they were not sure about the reaction of the parents. The young men seemed to be less worried than the young women about rejection by their family.
"Within Turkish families, there is a very strong bond. It is very difficult to break this bond. If you are in trouble like this (having HBV), they will not ostracise you. Even if you have done bad things... they will really regret it, it will break their heart, but they will not ostracize you because that is just not done." (G2 male participant)
The quote makes clear that young men feel strongly supported by their family. However, in some cases they perceived social interference of the family as a stressor, as there might be so much concern that they feel overwhelmed by it. Social support in G1 men was shortly discussed, but neither receiving nor giving support regarding HBV-testing provoked discussion.
Cultural factors
Issues related to the cultural realm that influence HBV-screening behaviour may be (1) the sensitivity regarding sexuality, (2) the issue of reputation and (3) the responsiveness to authority.
As for the sensitivity regarding sexuality, a shift was noted in the perception of HBV (testing) during the discussions: in most groups HBV infection was initially not seen as an STD and there was a positive attitude towards testing. Once aware of the routes of transmission (i.e. blood and sexual contact), the aspect of sexual transmission became the dominating issue, and social-cultural influences became apparent. However, when the discussions were summarized, participants seemed to return to their initial beliefs regarding HBV infection and testing. In all groups, sexuality was said to be a sensitive subject. G1 men mentioned as reason for not going for screening a sense of being ashamed for the suspicion of others (of having had extramarital sex). Even though they themselves would have a clear conscience, they still could be affected by this suspicion. The younger men seemed to be more confident about dealing with others' opinions about their sexual behaviour. The men from the disadvantaged area even mentioned that "we (the men) don't have the problem of virginity"'. When the groups talked about extramarital sex, it almost always considered men, not women (except young women who were sometimes thought to have sexual engagements too). G1 women did not seem to perceive infection through sexual contact as a personal risk, although they mentioned they could be indirectly affected by the sexual behaviour of their husbands. As discussed in the section 'social support', the sensitivity regarding sexual behaviour and HBV-testing was an important issue for G2 women.
Regarding the issue of reputation, the G1 men expressed that an established good reputation could protect them from social suspicion. If a man with a good reputation would have an HBV test, peers would look up to him in admiration because of his responsible action. That person might act as an example for others in that sense. The girls mentioned that if they would be blamed for bad behaviour by others, that would be terrible and a big shock for their parents. In G1 women groups, the issue of elderly people being ashamed for having HBV was mentioned. This was even apparent during the discussions; it was noticed that the older women were less open in sharing ideas about health and disease. Congruent with their remarks about social norms about HBV, women expressed that one's reputation should be less important than one's health, and that it should not be a hindrance to get tested.
In the group of the young women, the confrontation with a male physician was discussed, which seemed to be a barrier for some of the girls. A Dutch male doctor was preferred above a Turkish male doctor by some, while others saw doctors as professionals no matter ethnic background and gender. The young men in the disadvantaged suburb had strong opinions about the impact of having HBV (screening) on their reputation. When a young man would like to marry a girl, her parents might check his history. Either having the disease or having been screened, might be a blemish and a reason for not accepting him as future son-in-law. Not everyone in the group agreed with this opinion.
In order to explore further possible cultural influences, it was asked whether responsiveness to authority could be related to hepatitis B screening. Strikingly, in all groups the authority of the Municipal Public Health Services (MPHS) became the subject of discussion rather than the authority of community leaders or parents, as we had expected. Everyone agreed that when screening and/or vaccination would be obligatory, this would be a motivating factor for the Turkish community to comply. In some groups, it was expressed that an invitation would make it easier for individuals to participate in screening. Should they worry about their behaviour, then the invitation would release them from suspicion of the social environment.
"Well it has a bit to do with taboo, but now we have discussed it, I can go for screening without getting into trouble." (G2 male participant, disadvantaged area)
However, during the discussions on responsiveness to authority, almost all groups questioned the efficacy of the Dutch health care services. This new emerging theme was thoroughly discussed and the results are to be found under the heading 'Efficacy of Dutch health care services'.
Religious factors
Issues related to HBV-screening that were mentioned by the participants were also in the realm of religion. These may be (1) responsibility for one's health, (2) the concept of cleanliness and (3) the Islamic doctrine regarding health and disease.
Regarding religious feelings of responsibility for one's health, all groups except the G1 women expressed the importance of their religion for the choices they will make regarding their health. Without probing, the responsibility for one's personal health and for the health of one's (future) partner, family and other persons in the social environment were mentioned as reasons for testing.
For the G1 men, a group in which a religious leader participated, the concept of cleanliness was seen as a condition for living 'halal' (lawful), and was presented as the solution for the prevention of HBV infection.
"Our prophet says: cleanliness is half of the faith. If someone is not clean, he might not go to heaven. A person who lives according to the rules of our religion will be almost 100% sure of not getting this disease (HBV)." (G1 men)
This concept of cleanliness, living 'halal', includes hygienic cleanliness (washing hands, using own toiletries), but also not having extramarital sex, and seemed to be most poignant for both G1 and G2 men. In none of the women's groups were the words 'halal' or 'haram' (unlawful) mentioned.
Aspects of the Islamic doctrine regarding health and disease were discussed in the groups:
"It is written: you have to do all you can in order to cure a disease". (G1 men)
Furthermore, it was noted that Muslims are obliged to care for the body, in order to be able to return it to Allah in an unblemished state. The young men mentioned religion also in the context of fate. They felt that there was a limit to what one could do to prevent disease, and that getting ill, in a sense, is also fate. However, their peers remarked that this might never be a reason for not trying your best to stay healthy. One group of young men also mentioned that in religion, there is always forgiveness and a solution for bad behaviour. This was also deemed valid in the case of extramarital sex, and for this group, this conviction would help them to speak with their parents about their (perceived immoral) behaviour. The G1 women did not connect their religion to their behaviour. When asked for the connection between their religion and having or preventing hepatitis B, the main focus in both groups was that extramarital sex is forbidden. The women did not mention that religion can prescribe to act positively for one's health, while all other groups did so.
Efficacy of Dutch health care services
In almost all groups, the difference in quality of health care in Turkey and the Netherlands was discussed spontaneously. The participants felt that in Turkey there was more quality of care; doctors are willing to prescribe medication and to order tests for patients readily, while in the Netherlands doctors seem to be resistant to do so. G1 women and G2 men most strongly expressed their dissatisfaction:
"For 1 or 2 years, I am not seeing the GP anymore. If I have some complain, I think... well leave it, the only thing I will get is a painkiller. (...) I ask you: is that a way to be treated?!" (G2 male participant)
"It might be off-topic, but I really want you to write this down: in the Netherlands the health-sector is really badly organised. A human life is not truly valued." (G1 female participant)
In the groups in the disadvantaged area, besides doubts about the quality of care, there was also distrust towards the Dutch health care system. This seems to be related to a general unhappiness about the Dutch government. It was expressed that one would rather spend his money on health in Turkey than in the Netherlands, as "they (the Dutch government) just try to get money from me" (G2 male participant). Also there were strong opinions about the role of the government in the case of hepatitis B prevention. A few times it was said:
"If this is such an important disease why do we only hear about it now?" (G1 women)
None of the groups saw practical barriers in the accessibility of the testing facilities at the Municipal Public Health Services, although high costs were mentioned as a possible obstacle.
Conclusion
This study explored socio-cultural determinants related to hepatitis B screening, and their relevance for male and female first and second generation Turkish migrants in the Netherlands. Motivating factors were the (religious) responsibility for one's health, the perceived obligation when being invited for screening, and social support in being tested for HBV. Perceived barriers were the association of HBV screening with STDs or sexual activity, the perception of low control over one's health, and the perceived low efficacy of the Dutch health care services. Reputation could act as either a motivator or barrier.
The findings suggest that participation in HBV-screening will increase if people receive a personal invitation from the MPHS. When developing an intervention aimed at the promotion of HBV-screening, it seems worthwhile to appeal to feelings of responsibility for one's own health and that of others, which were expressed by all groups. To overcome stigmatization of hepatitis B as being a sexually transmittable disease, emphasis should be placed on the most common route of transmission in the Turkish population, i.e. by blood contact during birth. Especially for young, unmarried women this will take away a major barrier in coming forward for screening. The intervention should also address the perceived lack of control over one's own health, by empowering people in showing how they can positively contribute to their own health, that of their family and wider community. Particularly for men, HBV screening should be advertised as a positive health act, which could even improve their reputation. Last, the perceived low efficacy of the Dutch health care services should be tackled by clearly explaining the screening procedures.
While this qualitative study provides useful insight in the socio-cultural determinants related to HBV-screening and their underlying mechanisms, quantitative confirmation of these findings is necessary. We therefore plan to conduct a survey which, together with the qualitative data from this study, will provide the basis for the development of a culturally-appropriate intervention aimed at the promotion of HBV-screening in the Turkish-Dutch population in Rotterdam, the Netherlands.
Competing interests
This manuscript has not been published elsewhere and is not under submission elsewhere. There is no conflict of interest.
Authors' contributions
OZ, JHR and JM made substantial contributions to the conception and design of this study and revised the manuscript critically. YV organised the Focus Group Discussions, analysed the data, and drafted the manuscript. YV and HV were involved in data-interpretation and in revising the manuscript. All authors read and approved the final manuscript.