Prevention and early detection of cervical cancer in the UK Abstract
This literature review explores the prevention and early detection of cervical cancer in the UK. Current findings indicate that there is a risk for women under the age of 25 years, who may develop cervical cancer. There appears to be a gap in UK policy that may overlook these women, who are beneath the age for initial screening but exceed the age for vaccination. Despite the inextricable link between sexual activity and cervical cancer, cervical screening and sexual health promotion still appear to be disjointed, and the role of a sexually transmitted infection leading to the development of cervical cancer has not been emphasised enough in public health messages. Further training should be provided and its impact monitored, designed to address this anomaly in health promotion. There are many barriers to health promotion including, those of a societal, cultural and religious nature. Additional research is required to ascertain the types of educational and awareness interventions that would be most effective in promoting and encouraging positive sexual behaviours among young people, and to explore how these might be successfully implemented. Key words: Cervical cancer ■ Cervical neoplasms ■ Papillomavirus vaccines ■ Health promotion
■
Papanicolaou test
C
ervical cancer has been acknowledged as a sporadic outcome of a common sexually transmitted infection (STI) (Bosch et al, 2008). The aetiological association is restricted to the family of the human papillomaviruses (HPVs). HPV DNA can be identified in 99.7% of all cervical cancers, with HPV types 16, 18, 45 and 31 being the most frequent (Bosch and Iftner, 2005; Everett et al, 2011; . From a global perspective the World Health Organization (WHO) (2013a) contends that cervical cancer is the second most common worldwide affliction among women. Worldwide, cervical cancer is the fourth most frequent cancer in women with an estimated 530 000 new cases in 2012 representing 7.5% of all female cancer deaths. Of the estimated more than 270 000 deaths from cervical cancer every year, more than 85% of these occur in less developed regions. In developed countries, programmes are in place that enable women to get Claire Foran, Emergency Nurse, Dublin; Arthur Brennan, Senior Lecturer, Kingston University and St George’s University of London Accepted for publication: January 2015
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screened, making most pre-cancerous lesions identifiable at stages when they can easily be treated. Early treatment prevents up to 80% of cervical cancers in these countries. It is thought that the high mortality rate from cervical cancer globally (52%) could be reduced by effective screening and treatment programmes. The prevention of cervical cancer involves taking action to promote greater awareness of personal health to reduce the need for secondary or tertiary health care. Early detection of cervical cancer involves strategic initiatives that result in an earlier diagnosis, which may not otherwise have occurred (American Cancer Society, 2012). According to the Department of Health (DH) (2012a), early detection and treatment can prevent around 75% of cervical cancers from developing. The WHO (2015a) asserts that prevention and early detection offers the most cost-effective, longterm strategy for the control of such cancers. Cervical cancer has received recent attention in social media, most notably since the death of celebrity Jade Goody in 2009. The publication of information on cervical cancer for people obtaining the vaccination also increased in since the NHS implemented the use of the HPV vaccine in 2008 (Public Health England, 2015). Despite this attention, there continues to be an absence of clear information in the UK for the public about the prevention and early detection of cervical cancer. This has been supported in a survey by The Eve Appeal (2010) ,which found that 40% of women in the UK were unable to name any of the probable symptoms of cervical cancer. The study also found that only 1% of women were able to identify HPV as the factor causing cervical cancer (The Eve Appeal, 2010). There are potential barriers that may prevent women, from accessing information on cervical cancer. These include: a lack of awareness of cervical cancer, attitudes (towards sexual health, women’s health and perceived attitudes towards open discussion of sexual behaviours), misconceptions and individual beliefs (WHO, 2006; Wang et al, 2010). Anxiety and embarrassment have been identified as the main impediments to seeking help (The Eve Appeal, 2010; Tavafian, 2012). The DH’s Improving outcomes: a strategy for cancer (2011) highlighted the need for improvement in public information, primary prevention interventions and targeted campaigns to increase public awareness of symptoms and to encourage early presentation. Increased awareness of signs of cancer among the general public, nurses and health professionals, can influence the prevention of the disease (WHO, 2015b). Collectively
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Claire Foran and Arthur Brennan
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LITERATURE REVIEW considered, this epidemiological data of the number of women both globally and in the UK affected by cervical cancer and the documented disturbing deficits of women’s knowledge in relation to HPV appear to suggest that closer attention, further research and more of an emphasis in publications, is warranted in the areas of early detection, prevention and education (Abiodun et al, 2014).
Table 1. Summary of search strategy exploring the prevention and early detection of cervical cancer in the UK (2000-2013) Keywords used (single and combined) ■■ Cervical
A search strategy using specific key words including: ‘cervical cancer’, and ‘cervical neoplasms’, ‘prevention’ and ‘early detection’ was carried out. The search was refined to cover the period between 2000 and 2013, to elicit an evolving perspective of this health problem in the early part of the 21st century for the purpose of comparison with relatively contemporary literature. Results outside of the chosen time period were discarded, as were results that related to developing countries, as they did not represent the indicated population of women without HIV and AIDS in developed countries with access to health care and advice. The databases included in the literature review were: the Cochrane Library, CINAHL plus, Internurse, and NHS evidence. Quality-assured government websites that were accessed included DH and the National Institute for Health and Care Excellence (NICE). Professional websites that were accessed included Cancer Research UK, The Eve Appeal and Jo’s Cervical Cancer Trust (UK health charities). These were chosen as they are public information sites for the study population and are accessible to the public in the UK. The search incorporated international literature from Belgium, Iceland, and the USA to give a global perspective of the problem and allow comparison with trends in the UK. Table 1 summarises the search strategy.
Analysis Three main themes emerged from evaluating the literature on the prevention and early detection of cervical cancer in the UK: ■■ The early detection of cervical cancer with the use of cervical screening ■■ The prevention of cervical cancer with the use of the HPV vaccination ■■ The prevention of cervical cancer with the use of health promotion strategies in relation to sexual behaviours. Six studies were found to meet the criteria of the review and are summarised in Box 1.
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Early detection of cervical cancer using cervical screening Cervical cancer has a pre-invasive stage, known as cervical intraepithelial neoplasia (CIN), which can be detected through cervical screening. Cervical screening diminishes the risk of developing cervical cancer and has been found to prevent approximately 4500 deaths annually in the UK (DH, 2012a; Bryant, 2012). The NHS Cervical Screening Programme screens over 3 million women every year (Public Health England, 2014). A supporting retrospective, case-control study by Sasieni et al (2003) compared the effectiveness of cervical screening and
British Journal of Nursing, 2015 (Oncology Supplement), Vol 24, No 10
Number of relevant citations yielded
Literature type
Cochrane Reviews
4
Systematic reviews and meta-analysis
CINAHL plus
31
Studies, reviews clinical protocols, and systematic reviews
Internurse
18
Reviews and studies
NHS Evidence NICE website DH website
39
Clinical guideline documents, studies, audits and systematic reviews
cancer
■■ Cervical
Literature review search strategy
Search databases and websites
neoplasms ■■ Early prevention/ detection of cervical cancer ■■ Human papillomaviruses and cervical cancer
Box 1. Studies considered in the literature review Sasieni et al (2003) Bano et al (2008) Brabin et al (2011) Forster et al 2012 Mather et al (2012) Watson and Serrant-Green (2012)
estimated the benefits of screening at distinct intervals and at varying ages. The study evaluated the efficacy of annual, 3-yearly and 5-yearly screening intervals and projected the appropriate initial screening age from this result. A nonprobability quota sample examined the epidemiology of 3837 women between 1990–2001, diagnosed with stage 1B or worse cervical cancer aged 20–69 years (1305) and compared them with age-matched controls (2532). The data were obtained from group practices located across the UK, and the required information was gathered from an online database: the Exeter System. The study found that 5-yearly screening in women aged 55–69 years was 83% effective compared with 87% effectiveness for annual screening; in women aged 40–54 years, 3-yearly screening was 84% effective compared with 75% for 5-yearly screening and 88% for annual screening. In women aged 20–39 years, annual screening was found to be 76% effective, compared with 61% effectiveness for 3-yearly screening. A methodological strength of this study was the large sample size of women with cervical cancer stages 1B and upwards in comparison with age-matched controls. According to Biau et al (2008), when there is a large sample size it allows for greater credibility in the research, in comparison with smaller studies. However, a limitation of this study concerned its sampling method, which may not have accurately represented the entire population, as the chosen area of the study was not specified and few sociodemographic characteristics were provided. A further limitation of the study related to the risk of selection bias, as the sample selection procedure deployed a nonrandomised method (Torgerson and Torgerson, 2001). The findings of the following investigation appear to
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The prevention of cervical cancer with the use of the human papillomavirus vaccination Over 100 types of HPV have been identified and 40 of these infect the genital region (Forbes, 2008). A total of 13 types are acknowledged to be oncogenic, with types 16 and 18 causing over 70% of all cases of cervical cancer (Peate, 2009; Maine et al, 2011). HPV is the most common STI globally (Racktoo and Coverdale, 2009; Murphy and Mark, 2012) with approximately 80% of sexually active adults having been infected with one or more genital HPV types at some point in their lives (Peate, 2006). Given this, HPV vaccination is important in protecting individuals and the population against cervical cancer which can lead to longterm damage to health and wellbeing (WHO, 2015) One interesting trend to note is the younger the person, the greater the knowledge of the HPV vaccine and its protective effects against cervical cancer, although there are also some misinterpretations (Watson and Serrant-Green, (2012). This could be as a result of the implementation of the HPV vaccine in schools and its inclusion in sexual health education given before vaccination. This was corroborated in a hermeneutical, phenomenological pilot study by Watson and Serrant-Green (2012). The aim of the study was to assess schoolgirls’ attitudes towards and knowledge of the HPV vaccination and see if their knowledge influenced their desire to have the vaccination. A non-probability, convenience sample was
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used to study 74 girls, aged 12-13 years, from a selected school of mixed socioeconomic group students. Individual interviews were conducted to elicit their knowledge and understanding of HPV. The findings indicated that the study participants had assorted attitudes and different levels of knowledge. Following a presentation on HPV, the majority of participants appeared to have increased levels of knowledge (69% in comparison with 16.4% before the presentation). However, a greater number of the schoolgirls (15% in comparison with 7%) consequently misinterpreted the information regarding the HPV vaccine, and its role in the prevention of cervical cancer following the presentation (Watson and Serrant-Green, 2012). According to Lester (1999), the main methodological strength of such a study was the use of phenomenological research, as it allowed for participants to discuss their personal perspectives and belief systems in relation to the HPV vaccination. A methodological limitation was the use of interviews with younger participants, as a lack of understanding of the questions may have affected the results. Fox (2009) acknowledges that the personal nature of interviews may increase the chance of error, particularly when asking questions. Two people talking about sensitive issues may lead to different topics being discussed that are not related to the main question, and the way one person asks a question may be different to another person. School nurses’ perceptions of factors affecting the uptake of the HPV vaccination may indicate the clinical challenges they face in this type of health promotion among school-aged children. Brabin et al (2011) conducted a hermeneutical, phenomenological study into the factors school nurses perceived to affect uptake of the HPV vaccination in two primary care trusts in Manchester. A non-probability, judgmental sample of 33 school nurses participated in the study. The majority (28) were aged over 35 years and at band 5 or 6. The data collection comprised tape-recorded, semi-structured interviews that aimed to explore the factors influencing vaccination uptake, as perceived by the nurses. The study revealed that a number of factors impeded their health promotion efforts including a lack of managerial support, poor staffing levels and staff availability, time constraints, adverse parental attitudes and strained relationships between school nurses and educational institutions. A methodological strength of this study was that interviews allowed the researchers to obtain detailed information about personal feelings, perceptions and opinions. A limitation of the study may have been its one-sided findings, which suggested that all school nurses who participated appeared to have had a negative view of the factors affecting the uptake of the HPV vaccination. This may have prevented their health promotion efforts towards increasing the uptake of the vaccination.
Prevention of cervical cancer with the use of health promotion strategies in relation to sexual behaviours The WHO (2015c) has highlighted cervical-cancer prevention strategies to include the delivery of information on STIs and their transmission, the teaching of safer sexual
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indicate a higher rate of pathology among younger women when compared with the findings of abnormal changes in women of different age groups. A retrospective, crosssectional study conducted by Bano et al (2008) analysed the epidemiological data of women in the London Borough of Lewisham over a 1-year period (2003-2004). A non-probability consecutive sample was used to study 2793 women under the age of 25 to determine the incidence of CIN in this group. Data of the screening histories were extracted from cytopathology records, which were combined with colposcopy and biopsy results for evaluation. The results showed that in the 16–24 age group, there were increased numbers of abnormal papanicolaou smear tests (15%) in comparison with the 25–64 age group (6.9%). A total of 277 screenings presented with atypical cells with fluctuating grades of dyskaryosis: 208 exhibited mild dyskaryosis; 53 indicated moderate dyskaryosis; 16 revealed severe dyskaryosis and 7 out of 62 high-grade CIN lesions were diagnosed in women under 20 years of age. The methodological strength of the study was the use of a cross-sectional design to determine prevalence of cervical cancer and identify associations that could then be more meticulously studied, such as early onset of sexual intercourse (Mann, 2003). However, its methodological limitation was that the sample representation may have been compromised owing to the absence of reported sociodemographic characteristics, including social class and education in the Lewisham area, and also because at that time London had one of the highest under-18 year old conception rates in England and Wales (Office for National Statistics, 2010).
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n Cervical cancer has been acknowledged as a sporadic outcome of a common sexually transmitted infection n Human papillomavirus (HPV) DNA can be identified in 99.7% of all cervical cancers, with HPV types 16,18, 45 and 31 being the most frequent n Early detection and treatment can prevent around 75% of cervical cancers from developing n There appears to be a gap in UK policy that may overlook women under the age of 25, who are beneath the age for initial screening but exceed the age for HPV vaccination. n Barriers to accomplishing change exist in this area for nurses and health professionals in practice
practices, negotiation skills and raising awareness of HPV to reduce high-risk sexual behaviours. These sexual-health promotion strategies are designed to empower individuals to accept responsibility for their own health and equip them with the knowledge and skills to make decisions appropriately (Moya, 2002; Resnik, 2007). A retrospective, comparative study conducted by Mather et al (2012) investigated and compared the knowledge of vaccinated and unvaccinated women in relation to cervical screening guidelines, their own assumed vulnerability to cervical cancer, screening intentions and uptake, attitudes and commitment to safe sexual behaviours. A nonprobability, convenience sample comprising 193 female university students aged 18–30 years. The study participants showed a range of sociodemographic characteristics, including: religion, ethnicity, and the number of vaccination doses received. Of the 193 students, 119 were vaccine recipients. The participants completed online self-reported questionnaires. The investigation found that vaccinated women held more constructive (beneficial and productive) attitudes towards practising safer sexual behaviours. However, an additional finding was that fewer than 5% were able to identify screening guidelines; only 50% used barrier contraception when sexually active and, of that 50%, there was a 42% uptake of screening. A methodological strength of the study was the nature of the data collection, as online questionnaires allow for anonymity and a sense of social distance can be created by using the internet (Cantrell and Lupinacci, 2007). This is particularly important for such sensitive issues as sexual behaviours (Ong and Weiss, 2000). A limitation of the investigation concerned the possibility of subject selection bias, as women who had been vaccinated would need to have given informed consent and were therefore more likely to have gained a deeper knowledge regarding HPV than unvaccinated women. The following investigation appears to partially corroborate the previously mentioned findings that the differences in levels of knowledge in relation to HPV vaccination and protection against cervical cancer and awareness of cervical cancer screening guidelines. A prospective case-study design piece of research conducted by Forster et al (2012) examined the influence of the HPV vaccination on the sexual behaviours of adolescent
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girls. A non-probability, convenience sample of 1460 girls between the ages of 16–18 years was recruited from seven schools situated in London and the South East of England. The schools were located in known areas of deprivation and ethnic diversity (Forster et al, 2012). Data were collected from self-completed questionnaires, which sought to explore the impact of HPV vaccination on sexual behaviours. The study found no evidence to support the development of unsafe sexual behaviours among adolescent girls as a result of having the HPV vaccination or that they felt they were being encouraged to have sex. The findings also revealed no variation in the proportion of participants who were sexually active over a 6-month period following the vaccination (Forster et al, 2012). The methodological strength of this investigation was the use of a case-study design to gain insightful knowledge of each girl’s feelings and attitudes about intimate issues that had not been previously investigated in any depth. A limitation of the study was its use of convenience sampling as the sample may not have been representative of the wider population (Lunsford and Lunsford, 1995; Magnani et al, 2005) of adolescent girls, and may have been subject to bias
Discussion The key findings of the reviewed studies indicate a risk for women under the age of 25 years of developing cervical cancer and appear to identify a gap in UK policy suggesting that these women are overlooked. The reason for this being that they are beneath the age for initial screening, but exceed the age for vaccination (DH, 2010). The findings have also revealed that knowledge and awareness levels of HPV are limited in the public sector among general practices, community, sexual-health, school and practice nurses, and gynaecological nurses (Lamming and Beckett, 2011). Despite the inextricable link between sexual activity and cervical cancer (WHO, 2014) cervical screening and sexual health promotion still appear to be disjointed, and the role of STIs in the development of cervical cancer has not been adequately emphasised in public health messages (Waller et al, 2004; Agius et al, 2010). Further training should be provided and its quality monitored, designed to increase health professionals’ knowledge, awareness and confidence in relation to HPV and preventive strategies to help decrease the incidence of cervical cancer. This literature review emphasised the lack of knowledge in relation to HPV, as a result of inadequate information, education and awareness campaigns for the public. These were identified as significant factors that impede the prevention and early detection of cervical cancer. In the authors’ opinion accurate and consistent information and education regarding HPV should be provided to the public to assist the detection of cervical abnormalities, which may cause a decline in cervical cancer incidence. This could be achieved with outreach sexual health education being provided in schools and universities and disseminated more widely including through social networks which have popular appeal with the younger population. This could improve understanding and awareness of HPV tailored to the most at-risk group for developing HPV, namely
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KEY POINTS
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Conclusion Barriers to accomplishing change in this area exist for nurses and health professionals in practice. These include: a lack of confidence in their own abilities, feelings of embarrassment, fear of upsetting or offending service users and a lack of knowledge and understanding when addressing the issues related to HPV (WHO, 2006). Additional barriers centre on a lack of familiarity regarding sexuality, conservative attitudes toward sexuality and anxiety when addressing sexual concerns (Gott et al, 2004). However, it is not surprising that nurses in particular, as they spend a longer time with patients than other health professionals, encounter difficulty in discussing such sensitive topics when cultural, societal and some religious faiths have made the topics of sexuality and related issues taboo. However, the importance of providing safe, accessible and effective sexual health education to young people features strongly in this literature review and is further supported by health policy across the UK (DH, 2011; 2012a; DH and cross government, 2013). Additional research is required to ascertain the types of educational and awareness interventions that would be most effective in promoting and encouraging positive sexual behaviours among young people and how these might be successfully implemented in order to promote the prevention BJN and early detection of cervical cancer. Conflict of interest: none For a summary of the methods and key findings of the studies considered in this literature review, please contact the editor. Abiodun O, Olu-Abiodun O, Sotunsa J, Oluwole F (2014) Impact of health education intervention on knowledge and perception of cervical cancer and cervical screening uptake among adult women in rural communities in Nigeria. BMC Public Health 14(814) Agius PA, Pitts MK, Smith AMA, Mitchell A (2010) Human papillomavirus and cervical cancer: Gardasil vaccination status and knowledge amongst a nationally representative sample of Australian secondary school students. Vaccine 28(27): 4416–22. doi: 10.1016/j.vaccine.2010.04.038 American Cancer Society (2012) Cervical Cancer: Prevention and Early Detection. http://tinyurl.com/89fhldy (accessed 13 February 2015) Bano F, Kolhe S, Zamblera D et al (2008) Cervical screening in under 25s: a high-risk young population. Eur J Obstet Gynecol Reprod Biol 139(1): 86–9. doi: 10.1016/j.ejogrb.2007.08.020 Biau DJ, Kernéis S, Porcher R (2008) Statistics in brief: the importance of sample size in the planning and interpretation of medical research. Clin Orthop Relat Res 466(9): 2282–8. doi: 10.1007/s11999-008-0346-9 Bosch FX, Iftner T (2005) The aetiology of cervical cancer. National Health Service Cervical Screening Programme. http://tinyurl.com/ oh7fkqy (accessed 15 May 2015) Bosch FX, Burchell AN, Schiffman M et al (2008) Epidemiology and natural history of human papillomavirus infections and type-specific
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implications in cervical neoplasia. Vaccine 26(Suppl 10): K1–16. doi: 10.1016/j.vaccine.2008.05.064 Brabin L, Stretch R, Roberts SA, Elton P, Baxter D, McCann R (2011) The school nurse, the school and HPV vaccination: a qualitative study of factors affecting HPV vaccine uptake. Vaccine 29(17): 3192–6. doi: 10.1016/j.vaccine.2011.02.038 Bryant E (2012) The impact of policy and screening on cervical cancer in England. Br J Nurs 21(4): S4, S6–10. doi: 10.12968/bjon.2012.21. Sup4.S4 Cantrell MA, Lupinacci P (2007) Methodological issues in online data collection. J Adv Nurs 60(5): 544–9. doi: 10.1111/j.13652648.2007.04448.x Department of Health (2010) Clinical Practice Guidance for the Assessment of Young Women aged 20-24 with Abnormal Vaginal Bleeding. http://tinyurl. com/orlvg56 (accessed 15 May 2015) Department of Health (2011) Improving Outcomes: A Strategy for Cancer. http://tinyurl.com/pw4jyat (accessed 13 February 2015) Department of Health (2012a) Cervical screening http://tinyurl. com/7gvxef9 (accessed 13 February 2015) Department of Health (2012b) Spotlight on…Quality assurance reference centers. http://tinyurl.com/nfduwlg (accessed 13 February 2015) Department of Health and cross Government (2013) A framework for sexual health improvement in England. hhttp://tinyurl.com/csqda42 (accessed 13 February 2015) The Eve Appeal (2010) What women know: Report on awareness levels of cervical cancer amongst women in England. http://tinyurl.com/pjhmfxk (accesed 13 February 2015) Everett T, Bryant A, Griffin MF, Martin-Hirsch PP, Forbes CA, Jepson RG (2011) Interventions targeted at women to encourage the uptake of cervical screening. Cochrane Database Syst Rev (5): CD002834. doi: 10.1002/14651858.CD002834.pub2 Forbes K (2008) The HPV vaccination programme: Is Britain ready? British Journal of School Nursing 3(4):176-80 Forster AS, Marlow LAV, Stephenson J, Wardle J, Waller J (2012) Human papillomavirus vaccination and sexual behaviour: cross-sectional and longitudinal surveys conducted in England. Vaccine 30(33): 4939–44. doi: 10.1016/j.vaccine.2012.05.053 Fox N (2009) Using interviews in a research project. NHS National Institute for Health Promotion. http://tinyurl.com/ojeq8jx (accessed 18 May 2015) Grainger C (2010) Management of a death following HPV vaccination. British Journal of School Nursing 5(4):178-81 Gott M, Galena E, Hinchliff S, Elford H (2004) ‘Opening a can of worms’: GP and practice nurse barriers to talking about sexual health in primary care. Fam Pract 21(5): 528–36. doi: 10.1093/fampra/cmh509 Lamming T, Beckett G (2011) A brief guide to human papillomavirus vaccination. Practice Nursing 22(8): 410-5 Lester S (1999) An introduction to phenomenological research. http:// tinyurl.com/omogj58 (acessed 13 February 2015) Lunsford T, Lunsford B (1995) The research sample. Part 1: sampling. Journal of Prosthetics and Orthotics 7(3):105-12 Magnani R, Sabin K, Saidel T, Heckathorn D (2005) Review of sampling hard-to-reach and hidden populations for HIV surveillance. AIDS 19(Suppl 2): S67–72 Maine D, Hurlburt S, Greeson D (2011) Cervical cancer prevention in the 21st century: cost is not the only issue. Am J Public Health 101(9): 1549–55. doi: 10.2105/AJPH.2011.300204 Mann CJ (2003) Observational research methods. Research design II: cohort, cross sectional, and case-control studies. Emerg Med J 20(1): 54–60 Mather T, McCaffery K, Juraskova I (2012) Does HPV vaccination affect women’s attitudes to cervical cancer screening and safe sexual behaviour? Vaccine 30(21): 3196–201. doi: 10.1016/j.vaccine.2012.02.081 Moya C (2002) Life skills approaches to improving youth’s sexual and reproductive health. http://www.advocatesforyouth.org/storage/ advfy/documents/lifeskills.pdf (accessed 13 January 2015) Murphy J, Mark H (2012) Cervical cancer screening in the era of human papillomavirus testing and vaccination. J Midwifery Womens Health 57(6): 569–76. doi: 10.1111/j.1542-2011.2012.00207.x Office for National Statistics (2010) Conception statistics, England and Wales, 2008. http://tinyurl.com/ph7uts6 (accessed 19 May 2015) Ong AD, Weiss DJ (2000) The impact of anonymity on responses to sensitive questions. Journal of Applied Social Psychology 30(8): 1691-708 Peate I (2006) Nursing care and treatment of the patient with human papillomavirus. Br J Nurs 15(19): 1063–9. doi: 10.12968/ bjon.2006.15.19.22107 Peate I (2009) The introduction of the human papillomavirus vaccine— key issues. Br J Nurs 18(2): 86–9. doi: 10.12968/bjon.2009.18.2.37860 Public Health England (2014) About cervical screening. http://tinyurl. com/q7mtwao (accessed 13 February 2015) Public Health England (2015) NHS public health functions agreement 201415. http://tinyurl.com/kyucvoo (accessed 15 May 2015) Racktoo S, Coverdale G (2009) ‘HPV? Never heard of it’ students and the
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adolescents, especially after their first sexual encounters when levels of knowledge about sexual health will be at their lowest and will affect the behaviours young people adopt relating to sex. This is also when young people have numerous partners after sexual debut (Grainger, 2010). This would also help to strengthen the relationship between local health services and educational organisations, helping to ensure that young people are aware of the services (in the area of sexual and physical health) available to them. This would impact on their future help-seeking behaviours in such circumstances.
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LITERATURE REVIEW HPV vaccine. British Journal of School Nursing 4(7): 328-34 Resnik DB (2007) Responsibility for health: personal, social, and environmental. J Med Ethics 33(8): 444–5. doi: 10.1136/jme.2006.017574 Sasieni P, Adams J, Cuzick J (2003) Benefit of cervical screening at different ages: evidence from the UK audit of screening histories. Br J Cancer 89(1): 88–93. doi: 10.1038/sj.bjc.6600974 Tavafian SS (2012) Predictors of cervical cancer screening: an application of health belief model. In: Rajkumar R (ed) Topics on cervical cancer with an advocacy for prevention. http://tinyurl.com/ly69agn (accessed 18 May 2015) Torgerson CJ, Torgerson DJ (2001) The need for randomised controlled trials in educational research. British Journal of Educational Studies 49(3): 316–28 Waller J, McCaffery K, Wardle J (2004) Beliefs about the risk factors for cervical cancer in a British population sample. Prev Med 38(6): 745–53. doi: 10.1016/j.ypmed.2004.01.003 Wang X, Fang C, Tan Y, Liu A, Ma GX (2010) Evidence-based intervention to reduce access barriers to cervical cancer screening among underserved Chinese American women. J Womens Health (Larchmt) 19(3): 463–9. doi: 10.1089/jwh.2009.1422 Watson C, Serrant-Green L (2012) Exploring HPV awareness and
understanding before and after health education. British Journal of School Nursing 7(5):240-8 World Health Organization (2006) Comprehensive cervical cancer control. A guide to essential practice. http://tinyurl.com/q5qh345 (accessed 13 February 2015) World Health Organization (2013a) Comprehensive cervical cancer prevention and control: a healthier future for girls and women. http://tinyurl.com/ myn28uw (accessed 15 February 2015) World Health Organization (2013b) Guidelines for screening and treatment of precancerous lesions for cervical cancer prevention. http://tinyurl.com/ ppye38u (accessed 13 February 2015) World Health Organization (2014) Human Papillomavirus (HPV) and Cervical Cancer. http://tinyurl.com/prr9hnk (accessed 13 February 2015) World Health Organization (2015a) Cancer. http://tinyurl.com/3xkdq7x (accessed 13 February 2015) World Health Organization (WHO) (2015b) Cancer prevention. http:// tinyurl.com/yjhw24u (accessed 13 February 2015) World Health Organization (WHO) (2015c) Early detection of cancer. http://tinyurl.com/2bwlyk5 (accessed 13 February 2015)
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This literature review explores the prevention and early detection of cervical cancer in the UK. Current findings indicate that there is a risk for women under the age of 25 years, who may develop cervical cancer. There appears to be a gap in UK policy that may overlook these women, who are beneath the age for initial screening but exceed the age for vaccination. Despite the inextricable link between sexual activity and cervical cancer, cervical screening and sexual health promotion still appear to be disjointed, and the role of a sexually transmitted infection leading to the development of cervical cancer has not been emphasised enough in public health messages. Further training should be provided and its impact monitored, designed to address this anomaly in health promotion. There are many barriers to health promotion including, those of a societal, cultural and religious nature. Additional research is required to ascertain the types of educational and awareness interventions that would be most effective in promoting and encouraging positive sexual behaviours among young people, and to explore how these might be successfully implemented. Key words: Cervical cancer ■ Cervical neoplasms ■ Papillomavirus vaccines ■ Health promotion
■
Papanicolaou test
C
ervical cancer has been acknowledged as a sporadic outcome of a common sexually transmitted infection (STI) (Bosch et al, 2008). The aetiological association is restricted to the family of the human papillomaviruses (HPVs). HPV DNA can be identified in 99.7% of all cervical cancers, with HPV types 16, 18, 45 and 31 being the most frequent (Bosch and Iftner, 2005; Everett et al, 2011; . From a global perspective the World Health Organization (WHO) (2013a) contends that cervical cancer is the second most common worldwide affliction among women. Worldwide, cervical cancer is the fourth most frequent cancer in women with an estimated 530 000 new cases in 2012 representing 7.5% of all female cancer deaths. Of the estimated more than 270 000 deaths from cervical cancer every year, more than 85% of these occur in less developed regions. In developed countries, programmes are in place that enable women to get Claire Foran, Emergency Nurse, Dublin; Arthur Brennan, Senior Lecturer, Kingston University and St George’s University of London Accepted for publication: January 2015
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screened, making most pre-cancerous lesions identifiable at stages when they can easily be treated. Early treatment prevents up to 80% of cervical cancers in these countries. It is thought that the high mortality rate from cervical cancer globally (52%) could be reduced by effective screening and treatment programmes. The prevention of cervical cancer involves taking action to promote greater awareness of personal health to reduce the need for secondary or tertiary health care. Early detection of cervical cancer involves strategic initiatives that result in an earlier diagnosis, which may not otherwise have occurred (American Cancer Society, 2012). According to the Department of Health (DH) (2012a), early detection and treatment can prevent around 75% of cervical cancers from developing. The WHO (2015a) asserts that prevention and early detection offers the most cost-effective, longterm strategy for the control of such cancers. Cervical cancer has received recent attention in social media, most notably since the death of celebrity Jade Goody in 2009. The publication of information on cervical cancer for people obtaining the vaccination also increased in since the NHS implemented the use of the HPV vaccine in 2008 (Public Health England, 2015). Despite this attention, there continues to be an absence of clear information in the UK for the public about the prevention and early detection of cervical cancer. This has been supported in a survey by The Eve Appeal (2010) ,which found that 40% of women in the UK were unable to name any of the probable symptoms of cervical cancer. The study also found that only 1% of women were able to identify HPV as the factor causing cervical cancer (The Eve Appeal, 2010). There are potential barriers that may prevent women, from accessing information on cervical cancer. These include: a lack of awareness of cervical cancer, attitudes (towards sexual health, women’s health and perceived attitudes towards open discussion of sexual behaviours), misconceptions and individual beliefs (WHO, 2006; Wang et al, 2010). Anxiety and embarrassment have been identified as the main impediments to seeking help (The Eve Appeal, 2010; Tavafian, 2012). The DH’s Improving outcomes: a strategy for cancer (2011) highlighted the need for improvement in public information, primary prevention interventions and targeted campaigns to increase public awareness of symptoms and to encourage early presentation. Increased awareness of signs of cancer among the general public, nurses and health professionals, can influence the prevention of the disease (WHO, 2015b). Collectively
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Claire Foran and Arthur Brennan
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LITERATURE REVIEW considered, this epidemiological data of the number of women both globally and in the UK affected by cervical cancer and the documented disturbing deficits of women’s knowledge in relation to HPV appear to suggest that closer attention, further research and more of an emphasis in publications, is warranted in the areas of early detection, prevention and education (Abiodun et al, 2014).
Table 1. Summary of search strategy exploring the prevention and early detection of cervical cancer in the UK (2000-2013) Keywords used (single and combined) ■■ Cervical
A search strategy using specific key words including: ‘cervical cancer’, and ‘cervical neoplasms’, ‘prevention’ and ‘early detection’ was carried out. The search was refined to cover the period between 2000 and 2013, to elicit an evolving perspective of this health problem in the early part of the 21st century for the purpose of comparison with relatively contemporary literature. Results outside of the chosen time period were discarded, as were results that related to developing countries, as they did not represent the indicated population of women without HIV and AIDS in developed countries with access to health care and advice. The databases included in the literature review were: the Cochrane Library, CINAHL plus, Internurse, and NHS evidence. Quality-assured government websites that were accessed included DH and the National Institute for Health and Care Excellence (NICE). Professional websites that were accessed included Cancer Research UK, The Eve Appeal and Jo’s Cervical Cancer Trust (UK health charities). These were chosen as they are public information sites for the study population and are accessible to the public in the UK. The search incorporated international literature from Belgium, Iceland, and the USA to give a global perspective of the problem and allow comparison with trends in the UK. Table 1 summarises the search strategy.
Analysis Three main themes emerged from evaluating the literature on the prevention and early detection of cervical cancer in the UK: ■■ The early detection of cervical cancer with the use of cervical screening ■■ The prevention of cervical cancer with the use of the HPV vaccination ■■ The prevention of cervical cancer with the use of health promotion strategies in relation to sexual behaviours. Six studies were found to meet the criteria of the review and are summarised in Box 1.
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Early detection of cervical cancer using cervical screening Cervical cancer has a pre-invasive stage, known as cervical intraepithelial neoplasia (CIN), which can be detected through cervical screening. Cervical screening diminishes the risk of developing cervical cancer and has been found to prevent approximately 4500 deaths annually in the UK (DH, 2012a; Bryant, 2012). The NHS Cervical Screening Programme screens over 3 million women every year (Public Health England, 2014). A supporting retrospective, case-control study by Sasieni et al (2003) compared the effectiveness of cervical screening and
British Journal of Nursing, 2015 (Oncology Supplement), Vol 24, No 10
Number of relevant citations yielded
Literature type
Cochrane Reviews
4
Systematic reviews and meta-analysis
CINAHL plus
31
Studies, reviews clinical protocols, and systematic reviews
Internurse
18
Reviews and studies
NHS Evidence NICE website DH website
39
Clinical guideline documents, studies, audits and systematic reviews
cancer
■■ Cervical
Literature review search strategy
Search databases and websites
neoplasms ■■ Early prevention/ detection of cervical cancer ■■ Human papillomaviruses and cervical cancer
Box 1. Studies considered in the literature review Sasieni et al (2003) Bano et al (2008) Brabin et al (2011) Forster et al 2012 Mather et al (2012) Watson and Serrant-Green (2012)
estimated the benefits of screening at distinct intervals and at varying ages. The study evaluated the efficacy of annual, 3-yearly and 5-yearly screening intervals and projected the appropriate initial screening age from this result. A nonprobability quota sample examined the epidemiology of 3837 women between 1990–2001, diagnosed with stage 1B or worse cervical cancer aged 20–69 years (1305) and compared them with age-matched controls (2532). The data were obtained from group practices located across the UK, and the required information was gathered from an online database: the Exeter System. The study found that 5-yearly screening in women aged 55–69 years was 83% effective compared with 87% effectiveness for annual screening; in women aged 40–54 years, 3-yearly screening was 84% effective compared with 75% for 5-yearly screening and 88% for annual screening. In women aged 20–39 years, annual screening was found to be 76% effective, compared with 61% effectiveness for 3-yearly screening. A methodological strength of this study was the large sample size of women with cervical cancer stages 1B and upwards in comparison with age-matched controls. According to Biau et al (2008), when there is a large sample size it allows for greater credibility in the research, in comparison with smaller studies. However, a limitation of this study concerned its sampling method, which may not have accurately represented the entire population, as the chosen area of the study was not specified and few sociodemographic characteristics were provided. A further limitation of the study related to the risk of selection bias, as the sample selection procedure deployed a nonrandomised method (Torgerson and Torgerson, 2001). The findings of the following investigation appear to
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The prevention of cervical cancer with the use of the human papillomavirus vaccination Over 100 types of HPV have been identified and 40 of these infect the genital region (Forbes, 2008). A total of 13 types are acknowledged to be oncogenic, with types 16 and 18 causing over 70% of all cases of cervical cancer (Peate, 2009; Maine et al, 2011). HPV is the most common STI globally (Racktoo and Coverdale, 2009; Murphy and Mark, 2012) with approximately 80% of sexually active adults having been infected with one or more genital HPV types at some point in their lives (Peate, 2006). Given this, HPV vaccination is important in protecting individuals and the population against cervical cancer which can lead to longterm damage to health and wellbeing (WHO, 2015) One interesting trend to note is the younger the person, the greater the knowledge of the HPV vaccine and its protective effects against cervical cancer, although there are also some misinterpretations (Watson and Serrant-Green, (2012). This could be as a result of the implementation of the HPV vaccine in schools and its inclusion in sexual health education given before vaccination. This was corroborated in a hermeneutical, phenomenological pilot study by Watson and Serrant-Green (2012). The aim of the study was to assess schoolgirls’ attitudes towards and knowledge of the HPV vaccination and see if their knowledge influenced their desire to have the vaccination. A non-probability, convenience sample was
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used to study 74 girls, aged 12-13 years, from a selected school of mixed socioeconomic group students. Individual interviews were conducted to elicit their knowledge and understanding of HPV. The findings indicated that the study participants had assorted attitudes and different levels of knowledge. Following a presentation on HPV, the majority of participants appeared to have increased levels of knowledge (69% in comparison with 16.4% before the presentation). However, a greater number of the schoolgirls (15% in comparison with 7%) consequently misinterpreted the information regarding the HPV vaccine, and its role in the prevention of cervical cancer following the presentation (Watson and Serrant-Green, 2012). According to Lester (1999), the main methodological strength of such a study was the use of phenomenological research, as it allowed for participants to discuss their personal perspectives and belief systems in relation to the HPV vaccination. A methodological limitation was the use of interviews with younger participants, as a lack of understanding of the questions may have affected the results. Fox (2009) acknowledges that the personal nature of interviews may increase the chance of error, particularly when asking questions. Two people talking about sensitive issues may lead to different topics being discussed that are not related to the main question, and the way one person asks a question may be different to another person. School nurses’ perceptions of factors affecting the uptake of the HPV vaccination may indicate the clinical challenges they face in this type of health promotion among school-aged children. Brabin et al (2011) conducted a hermeneutical, phenomenological study into the factors school nurses perceived to affect uptake of the HPV vaccination in two primary care trusts in Manchester. A non-probability, judgmental sample of 33 school nurses participated in the study. The majority (28) were aged over 35 years and at band 5 or 6. The data collection comprised tape-recorded, semi-structured interviews that aimed to explore the factors influencing vaccination uptake, as perceived by the nurses. The study revealed that a number of factors impeded their health promotion efforts including a lack of managerial support, poor staffing levels and staff availability, time constraints, adverse parental attitudes and strained relationships between school nurses and educational institutions. A methodological strength of this study was that interviews allowed the researchers to obtain detailed information about personal feelings, perceptions and opinions. A limitation of the study may have been its one-sided findings, which suggested that all school nurses who participated appeared to have had a negative view of the factors affecting the uptake of the HPV vaccination. This may have prevented their health promotion efforts towards increasing the uptake of the vaccination.
Prevention of cervical cancer with the use of health promotion strategies in relation to sexual behaviours The WHO (2015c) has highlighted cervical-cancer prevention strategies to include the delivery of information on STIs and their transmission, the teaching of safer sexual
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indicate a higher rate of pathology among younger women when compared with the findings of abnormal changes in women of different age groups. A retrospective, crosssectional study conducted by Bano et al (2008) analysed the epidemiological data of women in the London Borough of Lewisham over a 1-year period (2003-2004). A non-probability consecutive sample was used to study 2793 women under the age of 25 to determine the incidence of CIN in this group. Data of the screening histories were extracted from cytopathology records, which were combined with colposcopy and biopsy results for evaluation. The results showed that in the 16–24 age group, there were increased numbers of abnormal papanicolaou smear tests (15%) in comparison with the 25–64 age group (6.9%). A total of 277 screenings presented with atypical cells with fluctuating grades of dyskaryosis: 208 exhibited mild dyskaryosis; 53 indicated moderate dyskaryosis; 16 revealed severe dyskaryosis and 7 out of 62 high-grade CIN lesions were diagnosed in women under 20 years of age. The methodological strength of the study was the use of a cross-sectional design to determine prevalence of cervical cancer and identify associations that could then be more meticulously studied, such as early onset of sexual intercourse (Mann, 2003). However, its methodological limitation was that the sample representation may have been compromised owing to the absence of reported sociodemographic characteristics, including social class and education in the Lewisham area, and also because at that time London had one of the highest under-18 year old conception rates in England and Wales (Office for National Statistics, 2010).
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n Cervical cancer has been acknowledged as a sporadic outcome of a common sexually transmitted infection n Human papillomavirus (HPV) DNA can be identified in 99.7% of all cervical cancers, with HPV types 16,18, 45 and 31 being the most frequent n Early detection and treatment can prevent around 75% of cervical cancers from developing n There appears to be a gap in UK policy that may overlook women under the age of 25, who are beneath the age for initial screening but exceed the age for HPV vaccination. n Barriers to accomplishing change exist in this area for nurses and health professionals in practice
practices, negotiation skills and raising awareness of HPV to reduce high-risk sexual behaviours. These sexual-health promotion strategies are designed to empower individuals to accept responsibility for their own health and equip them with the knowledge and skills to make decisions appropriately (Moya, 2002; Resnik, 2007). A retrospective, comparative study conducted by Mather et al (2012) investigated and compared the knowledge of vaccinated and unvaccinated women in relation to cervical screening guidelines, their own assumed vulnerability to cervical cancer, screening intentions and uptake, attitudes and commitment to safe sexual behaviours. A nonprobability, convenience sample comprising 193 female university students aged 18–30 years. The study participants showed a range of sociodemographic characteristics, including: religion, ethnicity, and the number of vaccination doses received. Of the 193 students, 119 were vaccine recipients. The participants completed online self-reported questionnaires. The investigation found that vaccinated women held more constructive (beneficial and productive) attitudes towards practising safer sexual behaviours. However, an additional finding was that fewer than 5% were able to identify screening guidelines; only 50% used barrier contraception when sexually active and, of that 50%, there was a 42% uptake of screening. A methodological strength of the study was the nature of the data collection, as online questionnaires allow for anonymity and a sense of social distance can be created by using the internet (Cantrell and Lupinacci, 2007). This is particularly important for such sensitive issues as sexual behaviours (Ong and Weiss, 2000). A limitation of the investigation concerned the possibility of subject selection bias, as women who had been vaccinated would need to have given informed consent and were therefore more likely to have gained a deeper knowledge regarding HPV than unvaccinated women. The following investigation appears to partially corroborate the previously mentioned findings that the differences in levels of knowledge in relation to HPV vaccination and protection against cervical cancer and awareness of cervical cancer screening guidelines. A prospective case-study design piece of research conducted by Forster et al (2012) examined the influence of the HPV vaccination on the sexual behaviours of adolescent
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girls. A non-probability, convenience sample of 1460 girls between the ages of 16–18 years was recruited from seven schools situated in London and the South East of England. The schools were located in known areas of deprivation and ethnic diversity (Forster et al, 2012). Data were collected from self-completed questionnaires, which sought to explore the impact of HPV vaccination on sexual behaviours. The study found no evidence to support the development of unsafe sexual behaviours among adolescent girls as a result of having the HPV vaccination or that they felt they were being encouraged to have sex. The findings also revealed no variation in the proportion of participants who were sexually active over a 6-month period following the vaccination (Forster et al, 2012). The methodological strength of this investigation was the use of a case-study design to gain insightful knowledge of each girl’s feelings and attitudes about intimate issues that had not been previously investigated in any depth. A limitation of the study was its use of convenience sampling as the sample may not have been representative of the wider population (Lunsford and Lunsford, 1995; Magnani et al, 2005) of adolescent girls, and may have been subject to bias
Discussion The key findings of the reviewed studies indicate a risk for women under the age of 25 years of developing cervical cancer and appear to identify a gap in UK policy suggesting that these women are overlooked. The reason for this being that they are beneath the age for initial screening, but exceed the age for vaccination (DH, 2010). The findings have also revealed that knowledge and awareness levels of HPV are limited in the public sector among general practices, community, sexual-health, school and practice nurses, and gynaecological nurses (Lamming and Beckett, 2011). Despite the inextricable link between sexual activity and cervical cancer (WHO, 2014) cervical screening and sexual health promotion still appear to be disjointed, and the role of STIs in the development of cervical cancer has not been adequately emphasised in public health messages (Waller et al, 2004; Agius et al, 2010). Further training should be provided and its quality monitored, designed to increase health professionals’ knowledge, awareness and confidence in relation to HPV and preventive strategies to help decrease the incidence of cervical cancer. This literature review emphasised the lack of knowledge in relation to HPV, as a result of inadequate information, education and awareness campaigns for the public. These were identified as significant factors that impede the prevention and early detection of cervical cancer. In the authors’ opinion accurate and consistent information and education regarding HPV should be provided to the public to assist the detection of cervical abnormalities, which may cause a decline in cervical cancer incidence. This could be achieved with outreach sexual health education being provided in schools and universities and disseminated more widely including through social networks which have popular appeal with the younger population. This could improve understanding and awareness of HPV tailored to the most at-risk group for developing HPV, namely
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KEY POINTS
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Conclusion Barriers to accomplishing change in this area exist for nurses and health professionals in practice. These include: a lack of confidence in their own abilities, feelings of embarrassment, fear of upsetting or offending service users and a lack of knowledge and understanding when addressing the issues related to HPV (WHO, 2006). Additional barriers centre on a lack of familiarity regarding sexuality, conservative attitudes toward sexuality and anxiety when addressing sexual concerns (Gott et al, 2004). However, it is not surprising that nurses in particular, as they spend a longer time with patients than other health professionals, encounter difficulty in discussing such sensitive topics when cultural, societal and some religious faiths have made the topics of sexuality and related issues taboo. However, the importance of providing safe, accessible and effective sexual health education to young people features strongly in this literature review and is further supported by health policy across the UK (DH, 2011; 2012a; DH and cross government, 2013). Additional research is required to ascertain the types of educational and awareness interventions that would be most effective in promoting and encouraging positive sexual behaviours among young people and how these might be successfully implemented in order to promote the prevention BJN and early detection of cervical cancer. Conflict of interest: none For a summary of the methods and key findings of the studies considered in this literature review, please contact the editor. Abiodun O, Olu-Abiodun O, Sotunsa J, Oluwole F (2014) Impact of health education intervention on knowledge and perception of cervical cancer and cervical screening uptake among adult women in rural communities in Nigeria. BMC Public Health 14(814) Agius PA, Pitts MK, Smith AMA, Mitchell A (2010) Human papillomavirus and cervical cancer: Gardasil vaccination status and knowledge amongst a nationally representative sample of Australian secondary school students. Vaccine 28(27): 4416–22. doi: 10.1016/j.vaccine.2010.04.038 American Cancer Society (2012) Cervical Cancer: Prevention and Early Detection. http://tinyurl.com/89fhldy (accessed 13 February 2015) Bano F, Kolhe S, Zamblera D et al (2008) Cervical screening in under 25s: a high-risk young population. Eur J Obstet Gynecol Reprod Biol 139(1): 86–9. doi: 10.1016/j.ejogrb.2007.08.020 Biau DJ, Kernéis S, Porcher R (2008) Statistics in brief: the importance of sample size in the planning and interpretation of medical research. Clin Orthop Relat Res 466(9): 2282–8. doi: 10.1007/s11999-008-0346-9 Bosch FX, Iftner T (2005) The aetiology of cervical cancer. National Health Service Cervical Screening Programme. http://tinyurl.com/ oh7fkqy (accessed 15 May 2015) Bosch FX, Burchell AN, Schiffman M et al (2008) Epidemiology and natural history of human papillomavirus infections and type-specific
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implications in cervical neoplasia. Vaccine 26(Suppl 10): K1–16. doi: 10.1016/j.vaccine.2008.05.064 Brabin L, Stretch R, Roberts SA, Elton P, Baxter D, McCann R (2011) The school nurse, the school and HPV vaccination: a qualitative study of factors affecting HPV vaccine uptake. Vaccine 29(17): 3192–6. doi: 10.1016/j.vaccine.2011.02.038 Bryant E (2012) The impact of policy and screening on cervical cancer in England. Br J Nurs 21(4): S4, S6–10. doi: 10.12968/bjon.2012.21. Sup4.S4 Cantrell MA, Lupinacci P (2007) Methodological issues in online data collection. J Adv Nurs 60(5): 544–9. doi: 10.1111/j.13652648.2007.04448.x Department of Health (2010) Clinical Practice Guidance for the Assessment of Young Women aged 20-24 with Abnormal Vaginal Bleeding. http://tinyurl. com/orlvg56 (accessed 15 May 2015) Department of Health (2011) Improving Outcomes: A Strategy for Cancer. http://tinyurl.com/pw4jyat (accessed 13 February 2015) Department of Health (2012a) Cervical screening http://tinyurl. com/7gvxef9 (accessed 13 February 2015) Department of Health (2012b) Spotlight on…Quality assurance reference centers. http://tinyurl.com/nfduwlg (accessed 13 February 2015) Department of Health and cross Government (2013) A framework for sexual health improvement in England. hhttp://tinyurl.com/csqda42 (accessed 13 February 2015) The Eve Appeal (2010) What women know: Report on awareness levels of cervical cancer amongst women in England. http://tinyurl.com/pjhmfxk (accesed 13 February 2015) Everett T, Bryant A, Griffin MF, Martin-Hirsch PP, Forbes CA, Jepson RG (2011) Interventions targeted at women to encourage the uptake of cervical screening. Cochrane Database Syst Rev (5): CD002834. doi: 10.1002/14651858.CD002834.pub2 Forbes K (2008) The HPV vaccination programme: Is Britain ready? British Journal of School Nursing 3(4):176-80 Forster AS, Marlow LAV, Stephenson J, Wardle J, Waller J (2012) Human papillomavirus vaccination and sexual behaviour: cross-sectional and longitudinal surveys conducted in England. Vaccine 30(33): 4939–44. doi: 10.1016/j.vaccine.2012.05.053 Fox N (2009) Using interviews in a research project. NHS National Institute for Health Promotion. http://tinyurl.com/ojeq8jx (accessed 18 May 2015) Grainger C (2010) Management of a death following HPV vaccination. British Journal of School Nursing 5(4):178-81 Gott M, Galena E, Hinchliff S, Elford H (2004) ‘Opening a can of worms’: GP and practice nurse barriers to talking about sexual health in primary care. Fam Pract 21(5): 528–36. doi: 10.1093/fampra/cmh509 Lamming T, Beckett G (2011) A brief guide to human papillomavirus vaccination. Practice Nursing 22(8): 410-5 Lester S (1999) An introduction to phenomenological research. http:// tinyurl.com/omogj58 (acessed 13 February 2015) Lunsford T, Lunsford B (1995) The research sample. Part 1: sampling. Journal of Prosthetics and Orthotics 7(3):105-12 Magnani R, Sabin K, Saidel T, Heckathorn D (2005) Review of sampling hard-to-reach and hidden populations for HIV surveillance. AIDS 19(Suppl 2): S67–72 Maine D, Hurlburt S, Greeson D (2011) Cervical cancer prevention in the 21st century: cost is not the only issue. Am J Public Health 101(9): 1549–55. doi: 10.2105/AJPH.2011.300204 Mann CJ (2003) Observational research methods. Research design II: cohort, cross sectional, and case-control studies. Emerg Med J 20(1): 54–60 Mather T, McCaffery K, Juraskova I (2012) Does HPV vaccination affect women’s attitudes to cervical cancer screening and safe sexual behaviour? Vaccine 30(21): 3196–201. doi: 10.1016/j.vaccine.2012.02.081 Moya C (2002) Life skills approaches to improving youth’s sexual and reproductive health. http://www.advocatesforyouth.org/storage/ advfy/documents/lifeskills.pdf (accessed 13 January 2015) Murphy J, Mark H (2012) Cervical cancer screening in the era of human papillomavirus testing and vaccination. J Midwifery Womens Health 57(6): 569–76. doi: 10.1111/j.1542-2011.2012.00207.x Office for National Statistics (2010) Conception statistics, England and Wales, 2008. http://tinyurl.com/ph7uts6 (accessed 19 May 2015) Ong AD, Weiss DJ (2000) The impact of anonymity on responses to sensitive questions. Journal of Applied Social Psychology 30(8): 1691-708 Peate I (2006) Nursing care and treatment of the patient with human papillomavirus. Br J Nurs 15(19): 1063–9. doi: 10.12968/ bjon.2006.15.19.22107 Peate I (2009) The introduction of the human papillomavirus vaccine— key issues. Br J Nurs 18(2): 86–9. doi: 10.12968/bjon.2009.18.2.37860 Public Health England (2014) About cervical screening. http://tinyurl. com/q7mtwao (accessed 13 February 2015) Public Health England (2015) NHS public health functions agreement 201415. http://tinyurl.com/kyucvoo (accessed 15 May 2015) Racktoo S, Coverdale G (2009) ‘HPV? Never heard of it’ students and the
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adolescents, especially after their first sexual encounters when levels of knowledge about sexual health will be at their lowest and will affect the behaviours young people adopt relating to sex. This is also when young people have numerous partners after sexual debut (Grainger, 2010). This would also help to strengthen the relationship between local health services and educational organisations, helping to ensure that young people are aware of the services (in the area of sexual and physical health) available to them. This would impact on their future help-seeking behaviours in such circumstances.
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LITERATURE REVIEW HPV vaccine. British Journal of School Nursing 4(7): 328-34 Resnik DB (2007) Responsibility for health: personal, social, and environmental. J Med Ethics 33(8): 444–5. doi: 10.1136/jme.2006.017574 Sasieni P, Adams J, Cuzick J (2003) Benefit of cervical screening at different ages: evidence from the UK audit of screening histories. Br J Cancer 89(1): 88–93. doi: 10.1038/sj.bjc.6600974 Tavafian SS (2012) Predictors of cervical cancer screening: an application of health belief model. In: Rajkumar R (ed) Topics on cervical cancer with an advocacy for prevention. http://tinyurl.com/ly69agn (accessed 18 May 2015) Torgerson CJ, Torgerson DJ (2001) The need for randomised controlled trials in educational research. British Journal of Educational Studies 49(3): 316–28 Waller J, McCaffery K, Wardle J (2004) Beliefs about the risk factors for cervical cancer in a British population sample. Prev Med 38(6): 745–53. doi: 10.1016/j.ypmed.2004.01.003 Wang X, Fang C, Tan Y, Liu A, Ma GX (2010) Evidence-based intervention to reduce access barriers to cervical cancer screening among underserved Chinese American women. J Womens Health (Larchmt) 19(3): 463–9. doi: 10.1089/jwh.2009.1422 Watson C, Serrant-Green L (2012) Exploring HPV awareness and
understanding before and after health education. British Journal of School Nursing 7(5):240-8 World Health Organization (2006) Comprehensive cervical cancer control. A guide to essential practice. http://tinyurl.com/q5qh345 (accessed 13 February 2015) World Health Organization (2013a) Comprehensive cervical cancer prevention and control: a healthier future for girls and women. http://tinyurl.com/ myn28uw (accessed 15 February 2015) World Health Organization (2013b) Guidelines for screening and treatment of precancerous lesions for cervical cancer prevention. http://tinyurl.com/ ppye38u (accessed 13 February 2015) World Health Organization (2014) Human Papillomavirus (HPV) and Cervical Cancer. http://tinyurl.com/prr9hnk (accessed 13 February 2015) World Health Organization (2015a) Cancer. http://tinyurl.com/3xkdq7x (accessed 13 February 2015) World Health Organization (WHO) (2015b) Cancer prevention. http:// tinyurl.com/yjhw24u (accessed 13 February 2015) World Health Organization (WHO) (2015c) Early detection of cancer. http://tinyurl.com/2bwlyk5 (accessed 13 February 2015)
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