Human papillomavirus infections and risks of cervical cancer: what do women know?
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1 HEALTH EDUCATION RESEARCH Vol.17 no Theory & Practice Pages Human papillomavirus infections and risks of cervical cancer: what do women know? Marian Pitts and Tracy Clarke 1 Abstract Human papillomavirus (HPV) is now known to be a risk factor for the development of cervical cancer. This study examines women s knowledge of cervical screening and dysplasia and HPV. The entire female work force of a mediumsized UK university received a questionnaire concerning knowledge of cervical screening, treatment for abnormalities and HPV. Four hundred women returned completed questionnaires. Knowledge of early cervical cancer detection and screening methods was good. However, risk factors for cervical cancer were not well known. Awareness and knowledge of HPV was very limited. Past experience of an abnormal smear result and colposcopy was significantly associated with good knowledge of cervical screening, but not with knowledge of HPV. It is essential to improve women s understanding of this area in the context of plans to include screening for HPV in the UK s national cervical screening programme. Introduction Human papillomavirus (HPV) is one of the most common causes of sexually transmitted infections. More than 60 types of HPV have been identified; about one-third of which can be spread through Australian Research Centre for Sex Health and Society, La Trobe University, 215 Franklin Street, Melbourne, Victoria 3000, Australia and 1 Centre for Health Psychology, Staffordshire University, Stoke on Trent, Staffordshire ST4 2DE, UK sexual contact. Several types of HPV can lead to genital warts, the most recognizable sign of genital HPV infection. There is now very well established evidence for a causal association between infection with certain types of HPV and the development of cervical cancer. Evidence from molecular studies have identified mechanisms by which high risk types of HPV contribute to carcinogenesis, while epidemiological studies indicate the HPV can be recovered from more than 95% of all cervical tumours. For high-risk HPV types prevalence rates are around 8 12% in women aged and decline to 2 5% in women over the age of 35 (Cuzick et al., 1998). However, infection in young women may be transient, whereas infections persist in older women, are more stable and show a closer association with cervical cancer. It is currently being considered whether HPV testing could be a useful adjunct to cervical cancer screening. Some researchers have already supported such a move (Meijer et al., 1997), but others advocate caution (Bonn and Bradbury, 1998). The UK National Health Service has introduced a pilot scheme to screen women for HPV if they have a mild or borderline cervical smear result; women who test positive for the virus will be fast tracked for further investigation and treatment (Wise, 2000). A recent systematic review of the role of HPV testing within a cervical screening programme identified a lack of knowledge about the psychosocial issues involved in providing cervical screening in general and HPV testing in particular [(Cuzick et al., 1999), p. 112]. The same review indicated that there were no studies that addressed issues of knowledge of risk and the consequences Oxford University Press All rights reserved
2 HPV infections and risks of cervical cancer of an abnormal smear test result. In the light of the UK s pilot scheme, there is a pressing need to examine what women know about HPV and the implications of revealing their HPV status. There have been few studies that examine knowledge of HPV. All are US-based studies and most sample only American university students. Ramirez et al. examined knowledge, beliefs and attitudes about HPV in a non-random sample of 110 female college students; 28% had never heard of HPV (Ramirez et al., 1997). A second study reported 87% of female university students enrolled on a public health course had never heard of HPV (Vail-Smith and White, 1992). Yacobi et al. randomly sampled 500 university students (Yacobi et al., 1999). Only 37% of those who responded had ever heard of HPV and the median score on a 13-point knowledge scale was 3. A recent study, which sampled both male and female first-year college students, reported 29.1% of males and 35.3% of females had heard of HPV infection of the cervix (Baer et al., 2000). The justification offered by these studies for using college students is that the prevalence of HPV is greatest in the age range However, as pointed out earlier, it is rather older women who face greater risk of cervical cancer from HPV. All studies so far have found relatively low knowledge of HPV, but did not examine knowledge of cervical cancer and cervical screening. Without this information it is difficult to assess whether there is a general lack of knowledge of cervical cancer, the role of screening and the role of HPV or whether there are specific gaps in the knowledge base. Thus, a study is required which is UK based, examines a wider educational range, includes older women, and examines the knowledge of HPV in the light of understanding about cervical cancer generally and the outcome of the screening process specifically. The study reported here examined, for the first time, knowledge of these elements within a population of mature women. Method Respondents The study population comprised 985 female employees at a university in the North West of England. This constituted the entire female workforce, and included academic, managerial, clerical, administrative and manual staff. Academic staff were from Schools of Art and Design, Humanities and Social Sciences, Sciences, Law, Management, Computing, and Engineering. Managerial, and administrative and clerical staff were from Student Services, Recruitment, Library Services, Estates, Catering and Residential Services. Procedure All female employees received a three-page selfadministered questionnaire via internal post, with a covering letter explaining the purpose and importance of the study and a return envelope. Participants were assured of complete anonymity in response to the answers provided. A general reminder was sent via 2 weeks after the posting and a final reminder was sent after a further week. Eight questionnaires were returned due to address unknown and two were returned uncompleted. Of the remaining 975 potential respondents, 400 returned completed questionnaires giving a response rate of 41%. Measures The 27-item questionnaire was developed to measure understanding of the purpose and mechanics of cervical screening, and to assess awareness and knowledge of HPV. The questionnaire was divided into four sections: A. A demographic section to obtain basic information about social background. Previous experience of a cervical smear test or colposcopy was established by asking Have you ever had a cervical smear test?, If yes, how often do you attend for cervical smear tests? and Have you ever had a colposcopy examination?. B. A section to assess knowledge of early cervical cancer detection and screening methods (smear tests and colposcopy) and knowledge about relevant female anatomy, using a multiplechoice format. Questions were developed from previous studies (Kincey et al., 1991; Massad et al., 1997). Table I includes those questions 707
3 M. Pitts and T. Clarke Table I. Knowledge of cervical smear testing among a university workforce sample n % What is a smear test? scraping to look for abnormal cells speculum in the vagina treatment for cancer test for a sexually transmitted disease don t know What is the recommended frequency for a smear test? annually every 3 5 years every 10 years don t know What do you think an abnormal smear result might mean? a abnormal, precancerous cells cancer infection other don t know What proportion of women receives an abnormal smear result? 1: : : : : left blank a Multiple responses allowed. Table II. Knowledge of colposcopy and risk factors for cervical cancer n % What is colposcopy? treatment for uterine cancer investigation of abnormal cells, biopsies same as a smear test for cancer don t know or left blank What does a colposcopy examine? a cervix vagina uterus don t know What proportion of women have to undergo colposcopy? 1: : : : : left blank Which of the following might increase the risk of cervical cancer? a failure to use condoms early age of first sexual intercourse smoking high number of sexual partners other a Multiple responses allowed or produced by participants. on cervical smear testing, participants were asked: What is a smear test? and invited to tick as many as applied, The recommended frequency for a smear test, What do you think an abnormal smear test result might mean? (tick as many as apply), What proportion of women receive and abnormal smear result?. Table II includes those questions on knowledge of colposcopy and risk factors for cervical cancer. They included What is a colposcopy?, What does it examine?, What proportion of women undergo colposcopy? and Which factors increase the risk of cervical cancer? (tick as many as apply). C. A series of questions to assess awareness and understanding of HPV, including signs and symptoms, routes of transmission, and potential long-term complications. Questions were presented in a multiple-choice format with supplementary open-ended questions. The questions can be found in Table III and the answers to open ended questions are summarized in Table IV. D. Questions to identify from which sources participants had acquired their information about cervical screening and HPV. The questionnaire was piloted on a volunteer sample of 20 female university employees to refine the wording of items. The correct responses for Sections B and C were totalled to obtain knowledge scores for cervical screening and for HPV, respectively. The maximum scores available were 24 for Section B and 22 for Section C, with a higher score indicating better knowledge. 708
4 HPV infections and risks of cervical cancer Table III. Knowledge of HPV among a university workforce sample n % Have you ever heard of the HPV infection? yes no If yes what do you know about it? good knowledge vague knowledge inaccurate or no knowledge How do you think HPV is contracted? sexually other route of contraction don t know or left blank Which of the following increase the risk of contracting HPV? a early puberty multiple sexual partners if partner has had multiple sexual partners early sexual activity failure to use condoms other Do you think HPV is... always symptomatic sometimes symptomatic never symptomatic don t know or left blank If symptomatic, what are the signs and symptoms of HPV? good knowledge (e.g. genital warts) vague knowledge (e.g. irritation) inaccurate knowledge or left blank Is HPV an infection which affects: only or mainly men only or mainly women both men and women don t know or left blank What are the long-term effects of HPV? good knowledge (e.g. cancer) vague knowledge (e.g. other long-term effects) inaccurate knowledge or left blank a Multiple responses allowed. Data analysis The data were analysed using the Statistical Package for the Social Sciences (SPSS). Basic descriptive statistics and frequency calculations were performed on all variables. Independent t-tests, analysis of variance (ANOVA) and post hoc comparison tests (i.e. Scheffé tests) were used to analyse the data. Stepwise multiple regression was performed as a supplementary analysis. Results The study sample Of the 400 women who participated, the mean age was 40 years (SD 10.19; range 19 64). Fifty-six percent (n 222) were married, 17% (n 67) cohabiting, 16% (n 64) single and 11% (n 47) were separated, divorced or widowed. Most women were of white European origin (95%, n 380) and 60% (n 242) of the sample had one or more children. Forty-eight percent (n 192) were in clerical/administrative roles, 27% (n 106) were academics/research staff, 16% (n 65) were in managerial or supervisory roles and 8% (n 32) were in manual occupations. Ninety-eight percent (n 392) had attended for at least one cervical smear test, with 66% (n 265) attending for smear tests every 3 years. Thirtytwo percent (n 128) had previously received an abnormal smear result and 19% (n 77) had previously had a colposcopy examination. Cervical smear testing Table I summarizes the responses to questions about cervical smear testing. On the whole, respondents understanding of cervical cancer screening and detection was good; 97.3.% (n 389) of respondents identified a smear test as a scraping to look for abnormal cells with a further 2.3% (n 9) identifying it as a test for a sexually transmitted disease. The majority (95.3%; n 381) was aware that the recommended frequency for a smear test is every 3 5 years in the UK. Respondents demonstrated good understanding of the potential causes of abnormal smear results with 97.3% (n 389) indicating precancerous cells as the main reason for an abnormal result, with a further 45.0% (n 180) also indicating infections as possible causes. Sixty-seven percent (n 268) under-estimated the proportion of women who receive an abnormal smear, with only 22.3% (n 89) identifying the correct proportion as 1:12 (Duncan, 1992). 709
5 M. Pitts and T. Clarke Table IV. Content summary of open-ended answers Level of knowledge n Written response What do you know about HPV? good knowledge 27 mentions either cancer or cervical cancer 31 mentions genital warts 9 mention sexually transmitted diseases vague knowledge 11 mentions warts 7 mentions smear tests 5 mentions sexually transmitted diseases, e.g. STD carried by men inaccurate answers 4 related to toxic shock, initials ring a bell, newspaper articles, Candida infection? other comments 13 nothing left blank 293 total 400 What are the possible signs and symptoms of HPV? good knowledge 18 warts 4 discharge/soreness/itching 4 irritation/discomfort 1 cauliflower like growths vague knowledge 4 pain 4 infection 2 lays dormant for years 1 bleeding between periods 1 pain during intercourse 1 difficulty conceiving 1 difficulty with intercourse inaccurate responses 2 fever, losing consciousness other comments 8 don t know or? no answer 349 total 400 What are the long-term effects of HPV? good knowledge 45 mentions cervical cancer explicitly, e.g. increased risk of cervical cancer, can lead to cervical cancer vague knowledge 16 mentions infertility e.g. may affect infertility, pelvic infection leading to infertility other 25 wrote either don t know or? left blank 314 total 400 Colposcopy Table II summarizes respondents answers to questions about colposcopy and risk factors of cervical cancer. Sixty-two point three percent (n 250) correctly identified a colposcopy, with a further 33.0% (n 132) being unsure. Fifty-eight point three percent (n 233) understood it was an examination of the cervix, whilst 7.3% (n 29) thought it was an examination of the vagina, 4.5% (n 18) an examination of the uterus and 34.8% (n 139) unsure. Again, a large percentage (40.3%; n 161) under-estimated the proportion of women who undergo colposcopy, with only 16.3% (n 65) identifying the correct proportion as one in fifty. Risk factors for cervical cancer Respondents were asked to identify factors they thought might increase the risk of developing cervical cancer. Of those who responded, only 27.8% (n 111) thought that failure to use condoms might increase the risk of cervical cancer 1 710
6 HPV infections and risks of cervical cancer Table V. Informants about cervical smears, colposcopy and HPV What sources have you relied on for n % information? Family and friends Your own GP Practice nurse Other health professionals Television Magazines/books Other Total 852 and less than half (45.0%; n 180) were aware of smoking as increasing risk. Most frequently endorsed risk factors were early age of first sexual intercourse (60.3%; n 241) and increased number of sexual partners (67.8%; n 271). HPV knowledge Table III summarizes subjects responses to questions about HPV. Respondents were asked whether or not they had heard of HPV. Respondents awareness and knowledge of HPV was very limited. Only 30.0% (n 120) had heard of the HPV infection prior to the survey and 70.0% (n 280) had not heard of HPV. Thus, only 30% of the total sample went on to answer more detailed questions concerning their knowledge of the virus. Participants were asked what do you know about HPV? and how do you think HPV is contracted?. Their replies were scored as showing good knowledge, vague knowledge, inaccurate knowledge or no knowledge. Of those completing these questions, 16.8% (n 67) demonstrated good knowledge of HPV. Examples of the detailed responses rated as displaying good knowledge include there are many different types of HPV, some types are associated with genital warts and others are associated with premalignant conditions or an infection, sexually transmitted implicated as a cause of cervical cancer. Responses displaying vague knowledge (5.8%; n 23) often identified HPV as some kind of sexually transmitted infection but were unaware of the potential link with cervical cancer, e.g. some kind of warts? or sexually transmitted disease. A small percentage showed inaccurate knowledge such as identifying HPV as a Candida infection or as associated with pelvic inflammatory disease. Most respondents (69.3%; n 277) did not know how HPV is contracted, with 30.3% (n 121) reporting sexual activity as the main route. Most frequently identified risk factors for contracting HPV were multiple sexual partners (33.8%; n 135), partner s multiple sexual partners (31.3%; n 125), failure to use condoms (26.3%; n 105), early sexual activity (18.0%; n 72) and early puberty (1.5%; n 6). Seventeen percent (n 68) of women were aware that HPV is sometimes symptomatic; however, only 6.8% (n 27) demonstrated good knowledge of the possible symptoms, reporting genital warts, sores and irritation. The majority (89.8%; n 359) did not know any signs and symptoms of HPV. Only 19.8% (n 79) of subjects identified HPV as an infection affecting both men and women. Only 11.3% (n 45) of respondents identified a potential link between HPV and cervical cancer in the long term. Table IV shows the range of responses coded as either correct, vague or inaccurate for each of the openended questions of the survey. Sources of information Table V summarizes the reported information sources about cervical screening and HPV. The most frequently used source was GPs (64.3%; n 257), followed by practice nurses (50.3%; n 201), family and friends (30.5%; n 122), magazines and books (29.3%; n 117), other health professionals (17.3%; n 69), and TV (10.0%; n 40). Cervical screening and HPV knowledge scores Total scores were calculated for Sections B and C of the questionnaire. The mean score obtained for Section B (smear testing and colposcopy knowledge) was (SD 3.68, n 400). Only 43.25% of the respondents completed Section C. The mean 711
7 M. Pitts and T. Clarke score for those completing Section C (HPV) was (SD 5.72, n 173). Scores on smear testing and colposcopy significantly correlated with scores for HPV knowledge (r 0.371, n 173, P 0.001). There were no significant correlations between age and cervical screening knowledge (r 0.049, n 400, P 0.329) or age and HPV knowledge (r 0.013, n 173, P 0.861). Subgroup differences Differences in cervical screening knowledge and HPV knowledge between subgroups of the sample were examined using independent t-tests and oneway ANOVAs. Analyses revealed significantly higher cervical screening knowledge scores for married women compared with those not married (t 2.049; d.f. 398; P 0.041). Women with children were also found to be significantly more knowledgeable regarding cervical screening than women without (t 3.113; d.f. 398; P 0.002). HPV knowledge did not differ significantly with marital status or having children. Occupational status appears to account in part for differences in HPV knowledge, with academic/research staff scoring higher on the HPV questionnaire than the other occupational groups (F 2.61, d.f. 395,3 P 0.053). This result just failed to reach statistical significance and post hoc Scheffé tests indicated no significant differences in HPV knowledge scores between academic/research staff and other occupational groups. Past experience variables related to knowledge scores Past experience with abnormal smear results and colposcopy account for differences in cervical screening knowledge scores. Women who had previously received an abnormal smear result scored significantly higher on the cervical screening questionnaire than those with no previous experience (t 2.699; d.f. 396; P 0.007). Also, a significant difference in cervical screening knowledge was found between women who had previously had a colposcopy examination and those who had not (t 3.617; d.f. 377; P 0.001). In the case of HPV knowledge, scores did not differ significantly by past experiences with abnormal smears or colposcopy. The frequency with which women attended for cervical smears did not significantly affect either cervical screening knowledge (F 0.752, d.f. 395,4, P 0.522) or HPV knowledge (F 1.24, d.f. 395,4, P 0.296). As a supplementary analysis, stepwise multiple regression was performed to identify variables best predicting knowledge for cervical screening and HPV. Variables entered into the regression equation included age, marital status, occupational status, frequency of attendance for smear tests, and previous experience with abnormal smears and colposcopy. Results indicated that neither cervical screening knowledge, nor HPV knowledge, could be predicted by variables in the regression model. Discussion Knowledge of cervical screening and colposcopy was generally quite good amongst these women. There was a marked tendency to underestimate the percentage of women who might experience a colposcopy, with more than 25% of respondents indicating a frequency of one in 25 or more. In contrast, understanding of the risk factors associated with cervical cancer was quite poor and women had little notion of prevention of cervical cancer other than early detection via screening. HPV is extremely poorly understood, with only 30% of respondents reporting ever having heard of it. In particular, even among those women who reported having heard of HPV, they were unaware of the symptomatology of HPV or that it can affect both men and women. Only 11.3% were aware that HPV could have long-term effects such as an increased risk of cancer. It is striking that the major sources of knowledge are medical and health professionals. The topics of cervical cancer and HPV, in particular, have yet to permeate the health sections of magazines and newspapers or to feature on television programmes. Issues such as breast cancer are much more widely covered now, but there remains a reluctance to deal openly with these more sensitive issues. 712
8 HPV infections and risks of cervical cancer Whilst knowledge of cervical screening and abnormalities is associated with being married and having children, there is no association between HPV knowledge and such characteristics. Furthermore, there was no significant correlation between age and any of the knowledge scores. Thus, greater knowledge of screening and abnormalities is likely to be related to the greater obstetric and gynaecological experience of women with children. The occupational differences failed to reach significance. Women with a history of abnormal smears were significantly more likely to have screening and abnormality knowledge, but again there was no association with HPV knowledge. HPV has not featured on the screening agenda as yet. The sample size of 400 compares very favourably with previous studies. The response rate of 40% was disappointingly low, but is nonetheless better than other studies (Ramirez et al., 1997; Baier et al., 2000). This is particularly the case given that reminders were general and delivered only via which could have reduced the likelihood of some sectors receiving them. Inspection of the response distribution does not, however, indicate any particular bias towards one occupational group. It is very likely that there is some sample bias towards women who have experienced cervical screening and abnormalities, since our rates are higher than we would expect (Duncan, 1992). This view is supported by the fact that the few women who returned the questionnaire uncompleted indicated it did not apply to them. For example, women who no longer used the cervical screening service as the result of a previous hysterectomy returned blank questionnaires. It is likely that those women who responded to the survey were particularly interested in the issues, possibly because of personal experience, and we suspect that in the general population, knowledge of these issues could be considerably lower still. The knowledge base is generally so low that we cannot, as yet, predict which factors might be of influence amongst those who do have some basic knowledge. What does this tell us? There are major gaps in women s knowledge and understanding of the role of HPV in cervical abnormalities. This lack of knowledge and the presence of misunderstandings could greatly impede the prospects for effective screening for HPV. It is important that women are informed of HPV without creating additional unnecessary anxiety. Previous work has shown women are highly anxious on receiving an abnormal smear test result (Wardle et al., 1995; Peters et al., 1999) and the receipt of a positive indication of HPV could compound this. The challenge to public health is to develop ways of communicating accurate information about HPV and the associated risks within cervical screening initiatives such that women understand both the prevention and management issues associated with these viruses. Notes 1. The efficacy of condoms to protect against HPV is once again the matter for scientific debate; with a recent workshop concluding there was no epidemiologic evidence that condom use reduced the risk of HPV; the report did find that condom use might afford some protection in reducing the risk of HPV-associated diseases, including...cervical neoplasia in women (Workshop Summary: Scientific Evidence on Condom Effectiveness for Sexually Transmitted Disease Prevention, 20 July 2001, NIAIFD, NIH, DHHS). References Baer, H., Allen, S. and Braun, L. (2000) Knowledge of human papillomavirus infection among young adult men and women: implications for health education research. Journal of Community Health, 25, Bonn, D. and Bradbury, J. (1998) The warts and all approach to tackling cervical cancer. Lancet, 351, 810. Cuzick, J., Meijer, C. J. L. M. and Walboomers, J. M. M. (1998) Screening for cervical cancer. Lancet, 351, Cuzick, J., Sasieni, P., Davies, P., Adams, J., Normand, C., Frater, A., van Ballegooijen, M. and van den Akker, E. (1999) A systematic review of the role of human papillomavirus testing within a cervical screening programme. Health Technology Assessment, 3, Duncan, I. D. (1992) NHS Cervical Screening Programme: Guidelines For Clinical Practice And Programme Management. National Co-ordinating Network, Oxford. Kincey, J., Statham, S. and McFarlane, T. (1991) Women undergoing colposcopy: their satisfaction with communication, health knowledge and level of anxiety. Health Education Journal, 50,
9 M. Pitts and T. Clarke Massad, L. S., Meyer, P. and Hobbs, J. (1997) Knowledge of cervical screening among women attending urban colposcopy clinics. Cancer Detection and Prevention, 21, Meijer, C. J. L. M., Rozendaal, L., van der Linden J. C., Helmerhorst, T. H. I. M., Voorhorst, F. J. and Walbloomers, J. M. M. (1997) Human papillomavirus testing for primary cervical cancer screening. In Franco, E. and Monsonego, J. (eds), New Developments in Cervical Cancer Screening and Prevention. Blackwell Science, Oxford, pp Peters, T., Somerset, M., Baxter, K. and Wilkinson, C. (1999) Anxiety among women with mild dyskaryosis: a randomised trial of an educational intervention. British Journal of General Practice, 49, Ramirez, J. E., Ramos, D. M., Clayton, L., Kanowitz, S. and Moscicki, A. B. (1997) Genital human papillomavirus infections: knowledge, perception of risk, and actual risk in a nonclinic population of young women. Journal of Women s Health, 6, Vail-Smith, K. and White, D. M. (1992) Risk level, knowledge, and preventive behavior for human papilllomaviruses among sexually active college women. Journal of American College Health, 40, Wardle, J., Pernet, A. and Stephens, D. (1995) Psychological consequences of positive results in cervical cancer screening. Psychology and Health, 10, Wise, J. (2000) UK Pilot scheme for HPV testing announced. British Medical Journal, 320, 600. Yacobi, E., Tennant, C., Ferrante, J., Naazneen, P. and Roetzheim, R. (1999) University students knowledge and awareness of HPV. Preventive Medicine, 28, Received on March 5, 2001; accepted on December 27,
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