Anogenital warts in Danish men who have sex with men

Abstract

To determine the prevalence of anogenital warts (AGWs) and concurrent sexually transmitted infections (STIs) in men who have sex with men (MSM), and their knowledge of human papillomavirus (HPV). Attitudes towards the HPV vaccine among MSM are explored. A web-based cross-sectional survey on AGWs, sociodemographic factors and sexual behaviour conducted in August 2009 in Denmark. Overall 25.2% of the 1184 respondents reported a prior or current episode of AGWs. The prevalence of AGW was significantly higher in homosexuals compared with bisexuals, in men with high levels of education and in those with a high number of sexual partners within the last year. MSM with a history of another STI reported a significantly higher prevalence of warts. More than 70% did not know what causes AGWs. If a free HPV vaccine were to be offered, 94.4% would like to receive it. These data suggest a high prevalence of AGWs in Danish MSM. The awareness of HPV is low; however, the acceptance of a HPV vaccine seems high.

Keywords

anogenital warts HPV men who have sex with men Denmark vaccination

INTRODUCTION

Anogenital warts (AGWs) or condylomata acuminata is the most common sexually transmitted infection (STI) in Denmark. More than 90% of AGWs are caused by human papillomavirus (HPV) types 6 and 11.^1,2 Besides these two, at least 28 other HPV subtypes are transmitted sexually.

HPV infection is associated with acquisition of other infections such as HIV,³ but literature on the prevalence of other STIs in men who have sex with men (MSM) with a history of genital warts is lacking.

HPV is causally linked with cervical and anal cancer and associated with penile, orophangeal and oral cavity cancer. The proportion of these cancers that are caused by HPV is however not fully established.⁴ Anal cancer is rare, but increasing in Denmark and worldwide.⁵ Subgroups such as MSM are at higher risk of anal cancer. In the USA, anal cancer in MSM is even more common than cervical cancer in women.^3,6 However, knowledge about HPV and anal cancer among MSM seems to be very low.^7–9

Gardasil^®, the quadrivalent HPV vaccine, has been shown to reduce the incidence of AGW in women and has since the beginning of 2009 been a part of the Danish Vaccination Program, where it is offered to 12-year-old girls. Results from clinical studies on the effect of Gardasil^® in reducing the incidence of AGW in men have not been published so far (NCT00090285). However, commencing in 2007 the Australian federal government began funding a voluntary programme to make the Gardasil^® vaccine available free of charge to women aged 12–26 years for a period of two years, with an ongoing vaccination programme for 12 and 13 years olds as part of the pre-existing high school vaccination programme. Since then, a decrease by one-fourth per quarter in diagnosed warts in women aged under 28 years has been seen. Heterosexual men are partly protected through herd immunity, and in Australia an average quarterly decrease of 5% have been observed in heterosexual men of all ages. No reduction among MSM has been seen.¹⁰

In the present study we investigate the self-reported prevalence of genital warts and other STIs in MSM, risk factors for acquiring genital warts, knowledge about HPV as the cause of warts and anal cancer and the acceptance of a HPV vaccination programme.

METHODS

Homo-, bi- and transexual men in Denmark were offered to participate in a web-based questionnaire. The study was announced in October 2009 on Danish websites primarily aimed at homo- and bisexual men (www.boyfriend.dk, www.stopaids.dk, www.outandabout.dk). Participation was anonymous and after completion, an email address could be entered to join a draw to win an iPhone. It was not possible to enter the same email address twice. Questionnaire information was available prior to participation in the survey. The functionality was tested and refined by a group of 10 persons including three MSM. The questionnaire comprised a maximum of 27 questions on sociodemographics, sexuality, knowledge of HPV, and prior STIs. The questions were inspired by former studies on sexual behavior.^11,12 A positive answer to prior or present AGWs elicited further question on warts. Exclusion criteria were female sex and heterosexuality, which led to termination of the questionnaire.

We checked the data for duplicates, and validity was assessed by looking at unlikely combinations of answers. We found four participants with answers that seemed unlikely (i.e. age 17 with a history of four STIs including HIV and infectious hepatitis), but not impossible, and thus we decided to include all of the participants in the analysis.

Data analysis was conducted using SAS software (version 9.2; SAS Institute, Cary, NC, USA). Descriptive analyses were done for all variables. To identify factors associated with AGWs, Pearson's chi-square and Fisher's exact test were carried out.

RESULTS

Characteristics

A total of 1184 MSM participated in the survey. Of these, 1150 had no missing answers. All respondents were included in the analysis.

Descriptive characteristics of the recruited sample are summarized in Table 1.

Table 1

Baseline characteristics of 1184 men who have sex with men participants

Age (median: 34 years, range: 15–88, SD 12.1)	n	%
Sexual orientation
Homosexual	957	80.8
Bisexual	223	18.8
Transexual	4	0.3
Education
Primary and lower secondary school leaving examination	120	10.1
Apprenticeship	182	15.4
Upper secondary school leaving examination	152	12.8
Short- or medium-cycle higher education	417	35.2
Long-cycle higher education	300	25.3
Other	12	1.0
Missing	1	0.1
Relationship status
Single	767	64.8
Monogamous relationship	261	22.0
Open relationship	156	13.2
Age of sexual debut (median 17 years, range: 12–60, SD 4.0) Still a virgin	22	1.9
Sexually transmitted infections
Chlamydia	188	15.9
HIV	124	10.5
Gonorrhoea	185	15.6
Syphilis	84	7.1
Genital herpes	48	4.1
Infectious hepatitis	73	6.2
Anogenital warts	298	25.2
None of the above	752	63.5

The vast majority of MSM was homosexual, approximately 20% were bisexual, and only four respondents were transexuals. The median age of participants was 34 years, the median age of sexual debut was 17 years, and only 22 persons reported being virgins.

STIs were common: AGWs, chlamydia and gonorrhoea being the most frequent. One hundred and twenty four (10.5%) of the participants reported being HIV-positive.

Educational level was high with more than 60% with a higher education. Several of the participants were too young to have reached their final level of education.

Anogenital warts

More than one in four reported a history of AGWs (Table 2). The warts were located at different sites: more than half had had warts around the anus, one-third on the penis and one-third in the rectum. Eight men reported warts in the urinary tract.

Table 2

Anogenital warts (only participants with history of anogenital warts included)

	n	%
Anogenital warts (total)	298	25.2
1 time	209	70.1
2 times	45	15.1
3 times	24	8.1
4 times	9	3.0
≥ 5 times	7	2.3
Duration of warts (median 4 months, range 1–114, SD 21.4) Location
Penis	106	35.6
Urinary tract	8	2.7
Around the anus	169	56.7
In the rectum	104	34.9
Other sites	13	4.4
Type of treatment
Ointment applied by the patient at home	128	43.0
Ointment painted on the warts by the doctor	171	57.4
Cryotherapy	90	30.2
Laser treatment	60	20.1
Surgical excision	61	20.5
No treatment	20	6.7
Treatment provided by
Practitioner	157	52.7
Specialist (i.e. dermatologist)	73	24.5
Sexual health clinic	107	35.9
Hospital, other departments	54	18.1
Sex while having anogenital warts
Yes	133	44.6
No	165	55.4
Use of condom while having anogenital warts
Always	230	77.2
Sometimes	44	14.8
Never	24	8.1

The disease was present for a median period of four months, but with a high variance; one reported having had warts more than nine years. More than half were treated by a practitioner who had painted podophyllin on the warts. One hundred and seven (35.9%) men were treated at a sexual health clinic, 73 (24.5%) had been referred to a dermatologist, and 54 (18.1%) were treated in a hospital setting. Finally, 20 responders had not received any treatment.

Nearly 70% reported self-esteem problems while having AGWs, and more than half (55.4%) did not have sex when having AGWs.

Factors associated with AGWs

A history of warts was significantly more frequent in men with a history of another STI. For previously diagnosed HIV, syphilis, gonorrhoea, chlamydia, herpes, and hepatitis the calculated P values were <0.001 (Table 3). Likewise, those with a greater number of sexual partners within the last year showed higher prevalence of AGWs. The percentage of participants with a history of AGWs rose with increasing age up to the age of 60 years. No association with relationship status was found.

Table 3

Factors associated with anogenital warts

	Warts n (% of total with warts)	No warts n (% of total with no warts)	P
Age (years)
15–29	70 (23.6)	378 (43.9)	<0.0001*
30–44	152 (51.2)	311 (36.1)
45–59	68 (22.9)	140 (16.2)
≥60	7 (2.4)	33 (3.8)
Sexual orientation
Homosexual	263 (88.3)	679 (78.6)	0.0003**
Bisexual	34 (11.4)	182 (21.1)
(Transexual)	1 (0.3)	3 (0.3)
Education
Primary and lower secondary school	18 (6.0)	94 (10.9)	0.0065**
Apprenticeship	36 (12.1)	143 (16.6)
Upper secondary school	31 (10.4)	115 (13.3)
Short- or medium-cycle higher education	122 (40.9)	293 (34.0)
Long-cycle higher education	86 (28.9)	211 (24.4)
Other	5 (1.7)	7 (0.8)
Relationship status
Single	189 (63.4)	557 (64.5)	0.1424*
Monogamous relationship	60 (20.1)	201 (23.3)
Open relationship	49 (16.4)	106 (12.3)
Number of partners within the last year
0–5	119 (39.9)	460 (53.2)	0.0001*
6–10	50 (16.8)	181 (20.9)
11–20	59 (19.8)	112 (13.0)
21–30	27 (9.1)	47 (5.4)
More than 30	43 (14.4)	64 (7.4)
Other sexually transmitted infections
Chlamydia – yes	77 (25.8)	111 (12.8)	0.0001*
Chlamydia – no	221 (74.2)	753 (87.2)
HIV – yes	72 (24.2)	52 (6.0)	<0.0001*
HIV – no	226 (75.8)	812 (94.0)
Gonorrhoea – yes	90 (30.2)	95 (11.0)	<0.0001*
Gonorrhoea – no	208 (69.8)	769 (89.0)
Syphilis – yes	41 (13.8)	43 (5.0)	<0.0001*
Syphilis – no	257 (86.2)	821 (95.0)
Genital herpes – yes	20 (6.7)	28 (3.2)	0.0094*
Genital herpes – no	278 (93.3)	836 (96.8)
Infectious hepatitis – yes	32 (10.7)	41 (4.7)	0.0002*
Infectious hepatitis – no	266 (89.3)	823 (95.3)

P values for comparison of the whole warts group with the whole no warts group is given for each variable

*P value: chi-square test; **P value: Fisher's exact test

Knowledge of HPV

The awareness of HPV was low. More than 70% did not know what caused AGWs. When told that HPV in most cases causes AGWs and then asked whether they knew that some HPV subtypes are associated with cancer, 66% answered no. Almost all respondents (94.4%) wanted to receive the HPV vaccine if it was free, with the benefit of preventing cancer being the most important factor.

DISCUSSION

AGWs are a common problem in MSM; about one-fourth of MSM reports a history of AGWs. This result is supported by previous studies on self-reported history of genital warts in MSM.^9,13 Treatment is challenging and longstanding, affecting self-esteem and sexual behaviour.

The study shows low awareness of HPV in a well-educated group and a willingness to receive the vaccine for free similar to previous studies. The median time of wanting to receive the vaccine is two years after sexual debut.⁸

Only 22 virgins participated in our study. The vaccine is most efficacious before sexual debut, making a targeted HPV vaccine for MSM difficult. One way to overcome this problem would be to offer the HPV vaccine to all children aged 12 years old, and not only to girls, as is the case in Denmark.

HPV by polymerase chain reaction testing shows a high presence throughout the age groups in HIV-negative MSM with no association with age,⁶ emphasizing that MSM are exposed to HPV for a longer time period than women. Cost-effectiveness studies have been made for the risk of cervical cancer in girls.^14,15 No calculation on diseases caused by HPV in the group of boys who will proceed to form a relationship with another man has as yet been conducted.

The age of the respondents and the distribution of homosexuals versus bisexuals correspond with another questionnaire survey on sexual behaviour in MSM in Denmark.¹¹ A history of AGWs was significantly more frequent in persons with more than 11 partners within the last year. Previous studies have shown the same association.^6,13,16

The positive association with increasing age in men until the age of 60 is also similar to another study.¹³ One study found a non-significant trend towards an association between HPV infection diagnosed by a swab from the coronal sulcus and the anal area and anal infection with chlamydia, gonorrhoea or herpes simplex virus.¹⁷ There is no literature available on self-reported STI and genital warts in MSM.

In all, 10.5% reported being HIV-positive compared with 8% in another Danish survey.¹¹ These results are higher than the 4–5% estimated HIV in the total Danish MSM population.¹⁸ It is plausible that some in doubt of being HIV-positive could have answered yes, because it was not possible to answer ‘I do not know’. 6.4% said to be HIV-positive and a further 3.5% did not know their HIV status in another study.⁸ The true prevalence and incidence of STIs in MSM in Denmark are difficult to estimate, because the number of MSM is unknown.

Only part of the high rate of AGWs in MSM can be explained by the immune-depleting function of HIV. Anoreceptive intercourse allows the anal mucosa to come in direct contact with an HPV-infecting source and thus probably facilitates HPV transmission. Co-infection with other STIs (e.g. gonorrhoea) may be another HPV facilitating factor. Interestingly, Gardasil^® vaccination trials in men have shown that MSM are more likely to develop genital warts following incident external genital HPV 6/11 infections than heterosexuals. We do not know why this is the case thus there are several intriguing areas for future research.

The study provided a chance of winning an iPhone. It is possible that some have participated in the survey in order to win the phone, without meeting the inclusion criteria. Some may be duplicate answers from the same individual, but it was not possible to enter the same email address twice. The sample is not representative of the MSM population in Denmark or the online MSM population. On the other hand by using a web-based questionnaire we were also able to reach persons that do not seek sexual health clinics. Being able to answer the questionnaire anonymously at home might have improved participants' willingness to give correct answers.

The risk of cancer is a far more serious complication of HPV than AGWs, and practically none of the respondents were aware of this. The poor knowledge of HPV, similar to other studies,⁸ the increase in anal cancer combined with the fact that the vaccine is currently only given to girls suggests reduced prospects of diminishing AGWs and HPV-related cancers in MSM.

CONCLUSION

Self-reported AGWs were highly prevalent among the respondents, affecting both self-esteem and sexual behaviour. Knowledge of HPV and HPV-related cancers were very poor. This combined with the fact that the quadrivalent HPV vaccine is currently only given to young girls indicates a gap in the prevention of AGWs and HPV-related cancers in MSM.

Footnotes

ACKNOWLEDGEMENTS

We thank Carsten Sand for kind intellectual support, Tine Rikke Jørgensen for aiding in all aspects of the current work, Andreas Habicht for skillful assistance with the statistical analysis, Jes Witting and Thomas Kristensen for assistance in developing the questionnaire.

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