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It was not until 1988 that the NHS cervical screening programme began; since then it has proved to be a successful scheme in the detection and prevention of cervical cancer saving 4500 lives per year (NHS Cervical Screening Programme 2008, Care Commission 2008). Despite the effectiveness of smear tests, evidence shows that only 80% of women with cervical cancer would have had cervical screening (Bloomfield 2007 cited in Gannon and Dowling 2008).
In 2007 2,828 new cases of cervical cancer were diagnosed in the UK, and worldwide there are 493,000 cases annually (Cancer research UK 2010a, Ashford and Collymore 2005). With the prevalence of cervical cancer increasing there are concerns with the uptake of cervical screening in the UK particularly among ethnic minority of women. Evidence by Moser et al (2009) has shown there is a low uptake of cervical screening in ethnic groups of women; British women were 1.35 to 3.42 times more likely to have a cervical smear in comparison with women from an ethnic minority. Although other factors such as age and socioeconomic as demonstrated in Moser et al (2009) have an impact on the uptake of cervical screening, ethnicity seems to be a significant influence. Cervical screening is offered to women aged 25-64 years old; for women aged 25-49 screening is at 3 year intervals and for women aged 50-64 it is every 5 years (DOH 2006). Although uptake of cervical screening is lower overall in ethnic minority groups, there are differences in the uptake between ethnic groups (Luke at al 1996, Webb et al 2004).
The aim of this literature review is to discover how the uptake of cervical screening can be increased amongst ethnic minority women in the UK. In doing so the literature review sets out to identify ethnic women's beliefs and attitudes towards cervical screening, identify and evaluate ethnic women's barriers to cervical screening and to evaluate the interventions used to increase the uptake of cervical screening.
A literature search was conducted using the search terms 'cervical smears', 'ethnic minorities', 'cancer' , 'screening' , 'barriers', 'knowledge' , 'women' , 'prevention', 'interventions' and UK. As individual search terms did not provide a fruitful result of papers that were relevant, these search terms were combined as follows:
cervical smears + women attitudes +UK
cervical cancer prevention and screening +ethnic groups,
cervical screening + interventions UK,
cervical cancer + ethnic minorities UK,
cervical screening + barriers UK
cervical screening knowledge + ethnic minorities
cervical smears + ethnic minorities
The combined search terms were used in the search strategies of CINAHL, MEDLINE-via PubMed, BNI, Google Scholar and PsycArticles (see Appendix 1)
A total of 11 studies (Appendix 2) were found with the inclusion criteria of primary research and research published after 1990. It was important that the literature reviewed old research as it was only in 1988 that national cervical screening was introduced and the issue of cervical screening in ethnic minorities has been on-going. Hence this enabled a comparison of how ethnic minority views on cervical screening have changed over time. The exclusion criteria were primary research published outside the UK. This was due to the unfamiliarity with methods of cervical screening outside the UK. The use of electronic searching did not yield as many research as hoped for, furthermore it was very hard to find research on interventions that were tested on ethnic minority groups of women.
Cervical cancer is the second most common cancer in women under age 35 in the UK (Bedford, 2009). As the name suggests cervical cancer is cancer of the cervix. The cervix (neck of the womb) is part of the female reproductive system and connects the uterus to the vagina. The cervix has many functions: during menstruation it allows the passage of blood flow and during childbirth it dilates for the baby to pass through the uterus and into the vagina (Cancer Research UK 2010b).
The cells of the cervix can develop to pre-cancerous changes known as dysplasia. Dysplasia (which is abnormal cells on the cervix) can be categorised using cervical intraepithelial neoplasia (CIN) classification (see Appendix 2). For this reason it is important that women have regular smears as early detection of cervical abnormalities can initiate treatment before cancer develops (Patient UK 2010).
There are two types of cervical cancers: squamous cell carcinoma and adenocarcinoma. Squamous cell carcinoma is the most common form of cervical cancer and accounts for 80- 90% of cervical cancers. Squamous cell carcinoma invades the squamous epithelium of the ectocervix (Dunleavey 2009). The other form of cervical cancer is adenocarcinoma, although less common as it accounts for only 10% in all cases it is considered to be the more severe than squamous cell carcinoma. (Dunleavy 2009, What is cervical cancer? 2011). Moreover the cervical smear is not designed to detect adenocarcinoma, however is mainly intended at detecting the early changes of squamous cell carcinoma (Poulsen 2005).As cervical cancer progresses slowly it may be asymptomatic, however as it advances the symptoms such as irregular bleeding, bleeding or pain after sexual intercourse and increased discharge may be a sign of cervical cancer Smeltzer et al (2009). According to Shiffman et al (1993) there is strong evidence to suggest that Human Papilloma Virus (HPV) causes cervical cancer, with types 16 and 18 deemed to be strongly associated with cervical cancer. Other risk factors include, smoking, number of sexual partners, age of first intercourse and use of oral contraceptives (Cancer Research UK 2009b).
From the literature it is apparent that internal barriers such as , beliefs, attitudes, embarrassment, and lack of knowledge have an influence on the uptake of cervical screening in ethnic minorities (Doyle 1991, Naish et al 1994, Box 1998, Thomas et al 2005, Abdullahi 2009). There seems to be a consensus about beliefs and attitudes of ethnic minority women and cervical screening. Naish et al (1994) investigated factors that deter women from attending there GP for cervical screening. A focus group of women from Turkish, Kurdish, Bengali, Chinese, Vietnamese, Punjabi and Urdu speaking women was conducted. It was found that most of the women shared fatalistic beliefs about cervical cancer. It was noted that "if you have it, then that is it and it would be better if were detected early" (Naish et al 1994, p.1127). Similarly a more recent study by Abdullahi et al (2009) also found Somali women had fatalistic beliefs about cervical cancer; however these beliefs stemmed from a religious view rather than a cultural view as described in Naish et al (1994). Using a purposive sample, Abdullahi et al (2009) recruited Somali women from Camden. Somali women commonly believed that cervical cancer was the will of God. This belief is further supported by participants in Box (1998) and Thomas et al (2005) study. Box (1998) aimed to seek the views and experiences of black and minority ethnic (BME) women on smear test screening for cervical cancer. The findings showed attitudes and beliefs about cervical cancer were linked with promiscuity and seen as a punishment from God. A woman in Box's study (1998, p.7 ) stated " cancer , yes it happens here, not with us we stay with our men". Therefore for some ethnic minority women there is a chance of being culturally and religiously stigmatised as a result of the belief that cervical screening is only appropriate for those who are promiscuous.
For most ethnic minorities with strong religious and cultural backgrounds there is a high importance attached to how women should behave when not married. The commitment to religion in ethnic minorities especially those from a Muslim and Christian background means for most women they have to maintain their virginity until married otherwise may be exposed to social consequences (Shripinda 2010). For example in Moroccan and Turkish groups women found to have lost their virginity can be killed in what is known as honour killing (Shripinda 2010). This view is still strongly upheld. Young Pakistani, Arabic and Greek orthodox females expressed resilient views on keeping the virginal state when entering marriage (Thomas et al 2005). Thomas et al's (2005) study revealed young Pakistani women suggested they would go for a cervical screening only if the screener was not from their cultural background as they feared of being found out. Likewise in Box's study (1998), sexually active unmarried women were afraid their doctor or receptionist could not be trusted as to the reason why they attended the GP.
The unanimity on beliefs and attitudes towards cervical cancer is not shared across all types of ethnic groups of women. Interestingly the views of African women beliefs about cervical cancer are derived from superstition (Thomas et al, 2005). The African women in Thomas et al's study (2005) believed cervical cancer was a taboo and that to mention cancer might cause the cancer to manifest. Furthermore cervical cancer was seen as a taboo more than other types of cancers. The evidence above provides a strong link between ethnic minorities cultural and religious beliefs as a barrier in cervical screening.
Another concern over cervical screening was the issue of embarrassment. The cervical smear test is invasive and for most ethnic women the procedure can be physically and psychologically uncomfortable (Box 1998, Abdullahi et al 2009). The issue of embarrassment is particularly important to Somali women. For them the issue of embarrassment arises from female gender mutilation (FGM). WHO (2010) explains FGM as the total or partial removal of the external female genitalia. FGM in most cultures is as result of both cultural, religious and refers to back to the ideology of maintaining premarital virginity. For some Somali women there is the anticipation of embarrassment as result of the reaction from the doctor or nurse taking the samples (Abdullahi et al 2009). Consequently Abdullahi et al (2009) brings an understanding as to how FGM acts as a deterrence for Somali women in cervical screening.
These studies (Naish et al 1994, Box 1998, Thomas et al 2005, Abdullahi 2009) have the use of focus groups in common. Though this suggests the appropriate use of focus groups in the study, it has its limitations. Parahoo (2006) states the disadvantage of focus groups is that dominant personalities can control the discussions. This was evident in Naish et al (1994), where it was noted that both Turkish and Kurdish women interacted spontaneously and informally compared to the other ethnic groups of women. This can affect the credibility of the study as the views of ethnic women perhaps only reflected those from Turkish and Kurdish backgrounds and not everyone else. Furthermore focus groups are not effective compared with in-depth interview in dealing with sensitive topics. For example in Abdullahi's study (2009) the issue of promiscuity was discussed with discomfort. This presents one of the prime issues within focus groups, where participants may feel less inclined to discuss sensitive issues out of fear of scrutiny and criticism from others within the group. This is reinforced by Groups Plus (2003) who states that sensitive topics are easily discussed if participants in the group all share the same problem.
The lack of knowledge of cervical screening is often prevalent in ethnic minority groups. Box (1998) identifies that there were misconceptions about the purpose of screening. Similarly Abdullahi et al (2009) found that Somali women failed to recognise the importance of cervical screening. This supports a previous study by Doyle (1991) which identified ethnic minorities' unawareness of both the importance and existence of cervical screening. Somali women disregarded cervical screening because there was no cervical screening in Somalia; the concept of preventative health was also unfamiliar. The concept of preventative health is unaccustomed in some cultures. Doyle (1991) suggests in the Asian communities the reliance on folk medicines meant screening was outside the traditional views of healing. The disregard towards preventative health is perhaps underpinned by religious beliefs. Thomas et al (2005) found that many ethnic groups felt it was important to turn to religion as a form of coping emotionally. There was a consensus amongst the groups that if things are left with God he resolves the problem.
Despite the lack of knowledge of cervical screening amongst ethnic groups, other groups are more knowledgeable. Guajarati women in Box's study (1998) were the only ones aware that cervical screening is able to detect pre-cancerous cells. Thomas et al (2005) found African groups were more able to identify cervical cancer as a commonly occurring cancer within their community. However age has an influential role on the amount knowledge that is embedded. Younger African-Caribbean participants had the least knowledge about cancer as there was a perception cancer affected older people (Thomas et al 2005).
It appears that Thomas et al's study (2005) has a methodological weakness. In their study they aimed to describe factors that act as barriers to effective uptake of breast and cervical screening. However the sample may not be representative of the target population as the sample consisted of men. Since men do not partake in breast and cervical screening, their inclusion may have distorted the findings, therefore reduces the transferability and credibility of the study. Regardless of this, Thomas et al's (2005) study shows the significance in the link between age and lack of knowledge in cervical cancer.
The lack of knowledge amongst ethnic minorities perhaps was as a result of language difficulties. If they were able to communicate and comprehend information they received then this could enhance their understanding and knowledge of cervical screening. The majority of ethnic women declared that translated information in their languages was often inadequate and difficult to make sense of (Naish et al 1994, Abdullahi 2009, Thomas et al 2005, Box 1998). The translated information was not only seen as a problem, but for some ethnic minority women who were illiterate translated information was still perplexing. As a result there was a preference for being told about the cervical test in their own languages rather than reading a translated script (Box 1998).
One major external barrier that was very frequently much expressed was the gender of the GP or screener. There were conceptions that if it was male practitioners that did the screening then women are less likely to uptake cervical screening. Some women in Box's study (1998) felt that their bodies should only be seen by their husbands and it were adamant that the smear taker should be a female. Similarly Somali women, felt that as Muslim, women having a male practitioner taking the smears is inappropriate. Abdullahi et al's (2009) study is significant in identifying and providing solutions to the barriers that discourages Somali women from up taking up cervical screening. This study is commended well on its originality as mentioned by Abdullahi (2009), and this was the only study investigating barriers to cervical screening that was found that focused on the views of Somali women. Conducting a study on Somali women brings new knowledge to this area of research as the Somali community do not lend themselves to research because they are seen to be 'invisible' compared to other Muslim ethnic minorities (Information centre about Asylum and Refugees ( ICAR) 2004).However, Naish et al (1994) found that both Kurdish and Turkish women did not mind male practitioners, as they are used to male doctors in their home countries. Nonetheless it appeared that a female practitioner still had more favour compared to that of a male practitioner.
From the evidence the preference for a female doctor is not only due to cultural or religious views but also due to the lack of understanding and insensitivity that male doctors display towards ethnic women having cervical smears. This is particularly demonstrated in Box et al's study (1998, p.7) where a women stated "the doctor was cross with me when I asked for the forceps (speculum) to be warmed, how would he feel if it was him?" However Thomas et al (2005) suggests that this poor relationship between practitioners and patients was due to poor communication skills. In Thomas et al's (2005) study BME women identified that the attitudes portrayed by their GP was very discouraging and at times it felt as if their GPs did not want them to be there. Moreover the issue of racism is problematic for ethnic minority women. For example in Box (1998) some of the Asian women were cited as being treated coldly by the smear taker because of their race. Health advocates noticed BME women were treated less favourably than white women and when smears were taken they were provided with less comfort (Box 1998).
Childcare issues also play an influential part in preventing ethnic women in up taking cervical smears. Naish et al (1994) found with many women, having children in the same room was very distracting. This view was also supported by Somali women who indicated the lack of childcare facilities was a barrier in attending cervical screening (Abdullahi et al 2009).
There is a link between the perceived lack of sterility of equipment and the uptake of cervical screening. The views expressed by some ethnic women were that the speculum was not hygienic and that this could be a cause of cervical cancer instead of the association with HPV (Box 1998). One woman expressed the following concern; "the cancer might be there [in the clinic] you never know they need to cover it with water, wash it all away I've never seen them do that" (Box 1998 , p.g 9). The view is also reiterated in Naish et al's (1994) study, where Chinese women were adamant that the use of unsterile equipment could induce infections. This demonstrates how important the lack of knowledge amongst ethnic minorities can affect the uptake of cervical smears.
Interventions that increase cervical screening
Interventions that increase cervical screening such as health promotion, education, invitations, psychological interventions and media interventions are examined below.
Kernohan (1996) investigated the effectiveness of community-based intervention to improve knowledge on the uptake of breast and cervical screening. The sample consisting of 1000 women from different ethnic backgrounds were involved in a health promotion intervention. The study focused on Bradford's main minority ethnic women (South Asian) and was concerned with the impact of health education programmes on the knowledge of cervical screening in South Asian women. Compared to the other ethnic groups South Asian women had the lowest level of knowledge on cervical smears, however their knowledge had considerably improved from 35.8% to 68.7% after the intervention. Kernohan (1996) study is noteworthy for depicting a positive correlation between health promotion and knowledge of cervical screening. However as this study was a pilot study this area of research would require further work in order to provide robust evidence. Furthermore kernohan (1996) did not look at the impact of increased knowledge on the subsequent rate of uptake.
Evidence from Abdullahi et al (2009) and Naish et al (1994) suggest that addressing barriers which deter women from having cervical smears can be used as interventions to increase cervical smear rates. The lack of knowledge of cervical screening is an apparent barrier in most ethnic women and a proposed solution would be to increase the levels of knowledge of cervical screening. Abdullahi et al (2009) suggests that education about the purpose of cervical screening is key to encouraging Somali women to attend for cervical screening. However, suggesting such solutions to overcome barriers to cervical screening without trial may be futile, since without some testing the solutions there remains a gap in understanding the impact of the intervention suggested by Abdullahi et al (2009).
More importantly Sabates and Feinstein (2006) investigated the role of education on the uptake of preventative health care, in this case cervical screening. Sabates and Feinstein (2006) suggest that educational effects on the uptake of preventative health results in raising the awareness of and the importance of having a regular health check and therefore the inclination to uptake preventative health checks. The study found that women enrolled in courses or training leading to qualifications had a positive impact on the probability of the uptake of cervical smears. Sabates and Feinstein's (2006) study provides further support to the socio-economic determinants of the uptake of screening. However, the effectiveness of this particular intervention is limited as women within ethnic minorities tend to not achieve the accolades of adult learning as a result of cultural demands. According to YWCA (2011) some black minority ethnic women are missing from the school register and are pulled out of school as a result of family duties to marital commitment.
A systematic review conducted by Forbes et al (2009) reviewed interventions targeted at women to encourage the uptake of cervical screening. It concluded that invitation letters and educational materials were the most effective types of interventions. However evidence from Stein et al (2002) suggests that invitation letters were not effective. Stein et al (2006) investigated the effectiveness of three methods of inviting women with a long history of non -attendance to undergo cervical screening. The methods of invitation were a telephone call from a nurse, a letter from a well-known celebrity and letter from the local NHS Cervical Screening Commissioner. A telephone call and a letter from a celebrity were ineffective. A letter from the commissioner resulted in a small increase in the uptake of cervical screening this was not statistically significant. Although Stein et al (2006) findings contradict that of Forbes et al (2009), this does not nullify the results of Forbes et al's (2009) study. The findings from Stein et al (2005) highlight one of the limitations of doing a single study. Egger et al (2001) argues a single study often fails to detect a statistically significance between interventions when in fact such difference may exists, therefore are more likely to produce false negative results. Moreover, in the hierarchy of evidence for interventions, systematic reviews are at the top as they are more likely to produce a strong and less-biased synthesis of findings that to show whether the intervention has an effective outcome (Melnyk and Fineout-Overholt 2010) . For this reason Forbes et al (2009) has a more valuable contribution towards knowledge on the interventions that increase the uptake of cervical screening.
The NHS cervical screening programme (2011) highlights that encouraging women through reminders such as invitation letters is exceptionally important; this may not be as effective in motivating ethnic minority women to attend cervical screening. Some ethnic minority women are more likely to ignore invitation letters if translation is unavailable ( Naish et al 1994). On the other hand, there is a link between planning when, where and how of making an appointment and the success rate in uptake of cervical screening. This is referred to as implementation intentions - the initiation of behaviour is determined if the conditions when, where and how are planned (Bartholomew et al 2011).This was demonstrated by Sheeran and Orbell (2000) who tested the concept of implementation intentions as a method to increase non-attendance in cervical screening. It was found that the participants who produced implementation intentions were much more likely to attend for a cervical smear test compared to the control group. This demonstrates how empowering women to have more control on the choices in arranging their appointments can significantly encourage the uptake of cervical screening. This supports Abdullahi et al 's (2009) study where it was identified that inconvenient appointment times were also considered to be a barrier. Consequently the use of implementation intention as an intervention is noteworthy of encouraging ethnic women to uptake cervical screening. Furthermore, an area of research that would increase existing knowledge is to investigate implementation intentions on ethnic minority women and subsequent uptake of cervical smears, in order to provide strong evidence for such intervention.
The media has potentially an important role on the uptake of cervical screening. Howe et al (2002) investigated the impact of a television soap opera on the NHS cervical screening programme. Using a retrospective analysis on information of the NHS cervical screening databases, during the 6 month of the storyline, the number of smears performed in women whose previous smears were compared to women who had smears taken previously that year. The storyline involved a character that missed her regular screening appointments; later she was diagnosed with cervical cancer and 6 weeks later she died. Howe et al (2002) found that there were substantial increases in the number of cervical smears- from 65 714 in 2001, to 79,712 in 2002, 19 weeks after the storyline. This demonstrates a significant link between the effects of media in motivating women to take up cervical screening. In support is the impact of a celebrity profile on uptake of cervical screening. The media coverage of Jade Goody from diagnosis of cervical cancer till death has been an influential motive for some women to uptake cervical screening. Parkers (2010) reports that, since the media coverage of Jade Goody's case, figures from NHS Rotherham showed an 80% improvement rate in the uptake of cervical screening.
From reviewing the literature it is apparent that increasing the uptake of cervical screening amongst ethnic minority women poses a challenging problem. Ethnic minority women are faced with internal and external barriers that play an important role on their non- attendance for cervical screening. It appears the internal and external barriers are interrelated. For instance the issue of embarrassment may arise as a result of being screened by a male practitioner, as well as FGM particularly in the case of Somali women as stated earlier. Moreover the culturally sensitive issues such as the loss of virginity still pays a price tag in many cultures and the stigmatisation attached towards it means some young ethnic minority women might feel reluctant to take up cervical smears.
Needless to say the extent to which a barrier act as a deterrent to the uptake of cervical screening is very much culturally dependent. Women from African cultures see cervical cancer as a taboo, where as in Asian cultures cervical cancer is perceived as a disease for those who are promiscuous. Additionally, the cultural attitudes and beliefs may be a stronger barrier than child care issues for some ethnic minority women, whilst the sterility of equipment may have a stronger influence than the issue of embarrassment.
The lack of knowledge was the most common barrier that was revealed and it appears this has not changed over the years amongst ethnic minority groups ( Box 1998, Thomas et al 2005 , Abdullahi et al 2009). From evaluating the interventions, it remains substantial that socioeconomic factors (lack of knowledge and education) are predictors in determining ethnic minority women attendance for cervical screening. For this reason, it would be beneficial for communities where ethnic minorities are prevalent to have health promotion projects that produce the awareness of cervical screening (kernohan 1996).
There was sufficient evidence to suggest language difficulties as an important factor in deterring ethnic minority women from the uptake of cervical screening. Though research has not tested the effect of bilingual services as an intervention to increase cervical screening, an area in practice that needs room for improvement is the use bilingual services and bilingual interpreters in the cervical screening recall system. Forbes et al (2009) research supports the use of invitation letters as an intervention to improve the uptake of cervical screening and currently still remains the most popular intervention used. Therefore a recommendation for practice would be for invitation letters to be printed in the languages of ethnic minorities.
What was interesting and surprising, was the issue of racism as a barrier to the uptake of cervical screening. The ethnic minority often experience health inequalities as a result of racism, karlsen (2007) reports racism can lead to differences in treatment and access to health promoting resources for the ethnic minority. This was reflected in Box (1998) where Asian women expressed their concerns of being treated coldly and treated indecently as a result of their race. This area highlights the need for a change within the health services offered to ethnicity minorities in the UK. More importantly a contribution to research would be to tackle racism as an intervention to encourage ethnic minority women in the uptake of cervical screening (Szczepura 2005).
Furthermore training needs to be put in place for health professionals to understand and embrace the forms of cultural and religious beliefs amongst ethnic minorities in order to reduce prejudice and discriminatory practices. This would be particularly important to women from ethnic minorities where FGM is seen as a custom practice. Denniston et al (2001) states FGM continues to take place in many cultures around the world; health practitioners and screeners need to be taught to take a sensitive and a considerable approach when screening women with FGM.
Sheeran and Orbell's study (2000) makes a positive contribution towards the issue of improving the uptake of cervical screening in women from ethnic minority groups. The use of implementation intentions seemed to have an effect on women in their attendance for cervical screening. Implementation intentions would be advantageous for some ethnic minority women. Planning when, where and how an appointment would address some of the barriers identified, including the gender of the screener, ensuring that a bilingual interpreter was present, so if needed information given could be clarified. Thomas et al (2005) implies that the planning of an appointment for ethnic minority groups, especially for those with religious festivals is important. Ethnic women given the chance to decide when their appointment should take place would eradicate inconveniences such as being invited for screening during Ramadan. However further research would be necessary to establish the effectiveness as well as the cost-effectiveness of using implementation intentions amongst ethnic minority women and the uptake of cervical screening.
To conclude, this literature review examined how to increase the uptake of cervical screening amongst ethnic minority women in the UK. The evidence discussed in this review has explored the internal barriers and external barriers that deter ethnic women in the uptake of cervical screening.
It is hard to change people's behaviour because of what we believe in and how this has shaped our social norms and values. Therefore to increase the uptake of cervical screening amongst ethnic minority groups remains complex and inconclusive. With the evidence examined in this review, the interventions (health promotion, education, implementation intentions, invitation letters and the media) to improve the attendance and uptake of cervical screening noticeably have an influential impact in encouraging women to uptake cervical smears. However, more rigorous research needs to be carried out to provide answers in order to encourage ethnic minority women in the UK and their uptake of cervical screening.
The limitations of this review were the inability to access unpublished and grey literature, therefore and so this review may have gaps in research. Although the papers reviewed were relevant, another potential limitation was, the searching strategies used did not yield as many results as expected as also searching for the literature itself proved to be difficult.
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