Pitts, Marian K. PhD*; Fox, Christopher BPsych, BA (Hons)*; Willis, Jon PhD*; Anderson, Jonathon MB, ChB, FRACGP, MSc (MedSci)†
From the *Australian Research Centre in Sex, Health and Society, La Trobe University, Melbourne, Australia; and †Carlton Clinic, Melbourne, Australia
J. Anderson has been involved in research sponsored by CSL Ltd., a vaccine manufacturer. He has also received a fee as a member of their advisory board.
Funded from a La Trobe University Health Sciences Faculty Grant.
Correspondence: Marian K. Pitts, PhD, Director, Australian Research Centre in Sex, Health and Society, La Trobe University, 215 Franklin Street, Melbourne, Victoria, 3000, Australia. E-mail: firstname.lastname@example.org
Received for publication February 6, 2006, and accepted May 18, 2006.
ANAL CANCER IS A RARE cancer with an age-adjusted incidence of 1.3 per 100,000 men and 1.5 per 100,000 women. The American Cancer Society estimates that nearly 4,000 men and women will be diagnosed with cancer of the anus, anal canal, and anorectum in 2005.1 The incidence of anal cancer has been increasing in the United States among men and women over the past 30 years.2 This increase is more dramatic among men, and this change is attributed in part to an increase in receptive anal intercourse as well as to an increase in numbers of lifetime partners.3 Anal squamous cell carcinoma cancer has been consistently shown to be higher in gay and other homosexually active men than in heterosexually active men.4,5 The incidence in homosexually active men is also higher than that for cervical cancer in women.6
It is now well established that infection with certain strains of the human papillomavirus (most commonly HPV-16 and HPV-18) is a necessary cause of anal cancer, like with cervical cancer.3,7 Although all who engage in receptive anal sex are at increased risk of contracting HPV, there is particular concern among gay men.8 As long ago as 2000, an article in the Lancet was recommending regular screening with an anal Pap test for all homosexually active men9; screening is particularly important because HPV lesions in men are overwhelmingly subclinical.10 There is now clear evidence that HIV-positive people are at increased risk of anal cancer.7,11 Grulich et al12 demonstrated increased rates of cancer of the anus in people with HIV infection who had not gone on to develop AIDS. Current smokers are also at particularly increased risk of anal cancer.3
A study published in 2002 established low levels of knowledge and understanding among women about HPV and its link with cervical cancer.13 We decided to carry out a parallel study on gay and other homosexually active men. A literature search revealed one study of knowledge of HPV and anal cancer among gay men and was mainly focused on HPV and genital warts.14 Studies of HPV knowledge have focused almost entirely on women and on the link with cervical cancer.13,15,16 Thus, we used the approach developed in studies of cervical cancer and HPV knowledge to examine gay men's knowledge of anal cancer and HPV.
Men attending a large gay community event (Midsumma) in Melbourne in January 2005 were approached and invited to participate in a short survey taking approximately 7 minutes to complete. The survey was presented on a clipboard and some privacy was afforded by providing a place for men to compete the survey. They returned the survey by placing it in a large ballot box. This recruitment method cannot yield a response or refusal rate; however, very few men (approximately one in 10), once approached, refused to participate.
The 64-item survey was based on a previous survey concerning HPV and cervical cancer.13 Questions were modified to concern anal cancer. The survey asked demographic questions concerning age, sexuality, educational level, and employment. It then asked about health service use and about knowledge, attitudes, and beliefs about anal cancer. The survey instrument was piloted on 10 gay men to ensure readability.
The data were analyzed using the Statistical Package for the Social Science (SPSS). Basic descriptive statistics and frequency calculations were performed on all variables. Independent t tests and χ2 tests were used.
In all, 384 men returned completed surveys; 93% gave post codes in Victoria. Their average age was 37 years (range, 16–67 years). Two thirds (67.3%) were in full-time employment and a further 19.4% worked part-time or casually. Five percent were students and 5.8% were unemployed. More than half (58%) had undergraduate or postgraduate qualifications. A total of 45.3% were single, and 47.4% were living with their partner. Ninety-two percent identified as gay, 4.8% as bisexual, and 3.2% as heterosexual. Twenty-four (6.4%) respondents were HIV-positive and a further 3.5% did not know their HIV status.
Respondents were asked how often they had visited their general practitioner or physician in the past 6 months. The average number of visits was 2.67, with 17.7% reporting no visits in the past 6 months. HIV-positive respondents reported more general practitioner visits (mean, 5 visits) than their HIV negative counterparts (mean, 2.54) or those who did not know their HIV status (mean, 1.92) (P = 0.678).
Respondents were asked whether they had visited a doctor specifically for a sexual health checkup; this is a common term in Australia and usually comprises a swab of the throat and anus and a urine test for chlamydia and gonorrhea along with a blood test for syphilis. A total of 10.2% indicated they had never had a sexual health checkup, 27.6% indicated they last had a sexual health checkup more than 1 year ago, with the remainder (62.2%) reporting a sexual health checkup within the past year.
HIV-positive men (4.2%) were significantly less likely than HIV-negative men (9.8%) to have never had a sexual health checkup (χ2 46.97, df = 8, P < 0.0001).
A total of 30.9% of the survey respondents reported they currently smoked. This is far higher than the average for Victorian adults; currently 16.6% of Victorian adults are regular smokers. There were no significant differences among the percentages of smokers who were HIV-positive, -negative, or of unknown serostatus.
Anal Cancer and Testing
In total, 53 men (14.3% of the sample) had had an anal Pap smear (HIV-positive men were more likely to have had an anal Pap smear test [29.2% vs. 13.6%, not significant]) A knowledge scale was constructed concerning anal smear tests and risks associated with anal cancer. One point was scored for each correct answer with a possible total of 12 correct answers. The mean score was 2.7 (standard deviation, 2.33) with a median of 2 and a mode of one. The range of scores was zero to 9. Nineteen percent of respondents scored zero. Table 1 summarizes the percentage of respondents who answered each knowledge item correctly. As can be seen, no item was correctly answered by more than half of respondents and awareness of risk factors was poor. Thirty-two percent were aware that smoking carried increased risk of anal cancer. Of most concern is the finding that only one in 5 men knew that being an anal-receptive partner increased risk of anal cancer.
Knowledge of Human Papillomavirus
Participants were then asked several questions concerning HPV. Table 2 summarizes the percentage correct responses for each item. These were combined to form an HPV knowledge scale with a possible maximum score of 8. Overall, participants scored a mean of 1.57, with a median of one; 47.1% scored zero. Fewer than half the sample had ever heard of HPV, the majority did not know whether it was ever symptomatic, and 56% did not know whether it affected men, women, or both.
Table 3 summarizes information sources concerning anal Pap smear tests. Of those respondents who had heard of an anal Pap smear test, most had heard of it in a doctor's office and less than 10% from any other source.
We asked respondents whether they used condoms with casual and regular partners. Overall, 72% reported always using a condom with casual partners; only 2% reported never using a condom with casual partners. The remainder reported mostly (15.9%), sometimes (4.6%), or rarely (1.7%) using a condom with casual partners. The pattern of condom use was markedly different regarding regular partners: 38.9% reported always using a condom with regular partners, 28.1% reported never using a condom with their regular partner(s), and 13.9% reported mostly, 7.7% sometimes, and 7.7% rarely using a condom with regular partner(s). These percentages are consistent with the findings from the Australian Gay Periodic Surveys conducted in similar settings.17
Knowledge of HPV and anal cancer was examined between subgroups of the sample using independent t tests and one-way analyses of variance. Analyses yielded few significant differences; there were no differences in knowledge associated with age, sexuality, or smoking. There were also no significant differences of HPV knowledge between those who consistently used condoms with regular or casual partners and those who did not. HPV knowledge was slightly, but not statistically significantly, higher among those men who had had an anal Pap test. HPV knowledge was significantly different according to level of education, with, not surprisingly, higher levels of education associated with higher levels of knowledge (r = 0.189, P < 0.0001; N = 382).
On a range of measures, it was clear that this well-educated sample knew very little about anal cancer and virtually nothing about HPV. Despite the fact that the majority had visited their general practitioner in the past 6 months and that most had had a sexual health checkup, they had not discussed anal cancer or the need for an anal test. Knowledge was somewhat better, although still poor, among those men at greater risk because of their HIV status.
These results must be treated with caution in some regard. This was a convenience sample recruited from a gay social event; it will be biased toward those homosexually active men who frequent gay social events. Such events are extremely popular in Australia and are very well established. Thus the sample is likely to be biased toward men who were connected to the gay community and who attended gay-focused health services. It was apparent to participants that the surveys were completely anonymous, and bias in responding to question resulting from fear of identification would be minimal.
Regular screening, probably every 3 years, for anal cancer among homosexually active men has been shown in an economic model to have an acceptable level of cost-effectiveness similar to many other public health programs compared with no screening.18 Goldie et al suggest that anal screening would be particularly beneficial and cost-effective for HIV-positive men.
Others have argued that routine anal cytology screening should not be instituted outside clinical trials until there is clearer evidence of effective treatments for anal intraepithelial neoplasia and better information on natural history.19
From these data, we can see that public awareness of anal cancer and HPV is extremely low and those at risk are unaware of the potential benefits associated with early detection of precancerous cells, i.e., anal intraepithelial neoplasia.
This study took place in Melbourne where a number of small studies of natural history and a phase I therapeutic vaccine study have taken place since 2002, which may account for the 14% of men who had ever had an anal Pap smear. Participants in that study were informed of the uncertainty about the meaning of anal cytology and the lack of evidence-based interventions.
A targeted health education campaign for homosexually active men and especially for those who are HIV-positive should be mounted if more widespread anal cytology screening is advocated; however, the current evidence does not support the implementation of a screening program for anal cancer in Australia. Moreover, it is important first to investigate general practitioners and other health professionals about their knowledge of the risk of anal cancer and HPV in relation to gay men. General practitioners, both those with a high caseload of gay men and those with more general population caseloads, can be trained to carry out this procedure and can act as an information source for gay men.
Finally, we know that a vaccine against some of the HPV strains that cause most cervical cancers has been shown to be highly effective, and it is likely that it will also protect against anal cancer.20 In Australia, the prospect of an HPV vaccine has been widely publicized recently because Professor Ian Frazer, who has developed the vaccine, is Australian of the Year for 2006. The media coverage, which began after the collection of data for this study has been entirely on the link between HPV and cervical cancer; there has been no mention of any link for men or with anal cancer specifically. Given the current levels of awareness among gay men, it will be some time before general practitioners are in a position to be able to offer either routine screening or prophylactic vaccination in an environment where true informed consent can be assured.
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