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Epidemiology
Genital warts in men: a large population-based cross-sectional survey of Danish men
  1. Christian Munk1,
  2. Ann Nielsen1,
  3. Kai-Li Liaw2,
  4. Susanne Krüger Kjaer1,3
  1. 1Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark
  2. 2Merck Research Laboratories, Merck & Co., Inc., Upper Gwynedd, Pennsylvania, USA
  3. 3Department of Obstetrics and Gynecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark
  1. Correspondence to Professor Susanne Krüger Kjaer, Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, Copenhagen Ø DK-2100, Denmark; susanne{at}cancer.dk

Abstract

Objectives To estimate the occurrence of and risk factors associated with genital warts in Danish men

Methods We conducted a cross-sectional, questionnaire-based study among almost 23 000 men aged 18–45 years, randomly sampled from the general population of Denmark. Data was collected on self-reported clinically diagnosed genital warts, and various lifestyle habits.

Results Ever having had clinically diagnosed genital warts was reported by 7.9% of the men. The median age at first occurrence was 22 years. Genital warts within the previous 12 months were reported by 0.92% of the men, with a peak of 1.83% among men aged 21–24 years. The likelihood of reporting genital warts was strongly correlated with the lifetime number of sex partners (OR 8.0; 95% CI 6.0 to 10.8 for ≥15 partners vs 1–2 partners). Other factors associated with an increased risk for genital warts included ever having smoked and having had other sexually transmitted infections.

Conclusions Almost 8% of Danish men aged 18–45 years reported having had a diagnosis of genital warts. The results provide baseline information for developing and monitoring prevention strategies against genital warts, such as vaccination against human papillomavirus types 6 and 11.

  • Genital Warts
  • HPV
  • Epidemiology (Clinical)

https://doi.org/10.1136/sextrans-2012-050512

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    Introduction

    Infection with human papillomavirus (HPV) causes morbidity among both men and women. Genital infection with oncogenic or high-risk types of HPV is the causal factor in cervical cancer, and HPV infection is also related to a number of other anogenital cancers (eg anal cancer, penile cancer and vulvar cancer) and to certain types of head-and-neck cancer.1 HPV types 16 and 18 cause approximately 70% of all cervical cancers. Genital warts are also caused by genital infection with HPV. The commonest HPV types involved are the non-oncogenic or low-risk types 6 and 11, which cause about 90% of all genital warts. Although genital warts are not life-threatening, they still cause a substantial amount of morbidity. The symptoms include itching and pain, and genital warts can also cause considerable embarrassment and psychosocial distress.2 ,3 Furthermore, genital warts can be difficult to treat, and relapses are common after treatment.

    Hu and Goldie recently estimated the economic burden of non-cervical HPV-6, -11, -16 and -18-associated lesions in the USA,4 with an annual cost of about US$ 418 million (range, US$ 160 million to US$ 1.6 billion), of which approximately 40% was for diagnosing and treating genital warts. Other studies have also reported that the economic burden of genital warts is substantial.5–7 So, apart from the individual consequences of having genital warts, the economic burden is also substantial.

    Two vaccines against HPV are available: a bivalent vaccine against HPV16 and 18, and a quadrivalent vaccine against HPV-6, -11, -16 and -18. The quadrivalent vaccine has been licensed in several countries for use in females aged 9–26 years. Studies on the efficacy of this vaccine for preventing anal precancerous lesions in men are showing promising results,8 and the USA Food and Drug Administration recently approved use of the vaccine for preventing genital warts in males aged 9–26 years and also for preventing anal cancer.9 ,10 Vaccination could potentially markedly reduce transmission of genital HPV infection, including genital warts.

    Although genital warts are considered to be common, few studies of their prevalence and incidence in the general population have been conducted. In a recent questionnaire survey of women (18–45 years) in the general population in four Nordic countries, more than 10% reported having had genital warts.11 Studies in men in the general population are even scarcer. A study in Australia showed a lifetime cumulative incidence of 4.0% in men aged 18–59 years,12 and in Slovenia, a low cumulative incidence of 0.4% was reported.13 Studies on genital HPV infection based on the presence of HPV DNA in genital swabs from men in the general population showed that the infection is highly prevalent with differences populationwise.14–17

    The aim of the study reported here was to estimate the occurrence of genital warts in a representative random sample of men in the general population of Denmark, and to determine the factors associated with self-reported clinically diagnosed genital warts.

    Material and methods

    Study population and data collection

    All residents of Denmark have a unique personal identification number, which contains information on gender and date of birth. The number is used as the key identifier to register all residents of Denmark in the national computerised Central Population Registry, with data on migration, current and former addresses and vital statistics. We took a random sample of men aged 18–45 years from the Registry. The study was approved by the Danish Data Protection Board.

    Between November 2006 and June 2007, we invited 33 000 Danish men to participate in the study. A total of 487 men were ineligible for the study because they had emigrated, did not speak Danish, had severe mental disability, or had died before contact, leaving 32 513 potential participants. Of these, 23 080 men (71.0%) participated in the study; 3835 men refused to participate, and 5598 did not respond to the study invitation. We excluded 101 men for whom a discrepancy was found between their personal identification number and their self-reported age. We also excluded 79 men who did not answer the question about genital warts. Thus, 22 900 men were available for analysis.

    An invitation and a paper-based self-administered structured questionnaire were posted to each potential participant. Men could respond either by returning the completed paper-based questionnaire, or by means of a password-protected identical web-based questionnaire. Men who did not respond within 3 weeks received a reminder, and those who still did not respond after the second invitation were contacted by telephone and encouraged to participate in a telephone interview, or to return the questionnaire. The telephone interview comprised the same questions as in the paper- and web-based questionnaires.

    The questionnaire contained questions on several aspects of lifestyle, including sociodemographic factors (eg marital status and schooling), smoking and alcohol intake (eg, age at start, number of cigarettes/drinks per day), condom use and sexual habits (eg, age at first sexual intercourse and number of sexual partners). We only asked about sex with female partners, and did not collect data on sex with male partners. Data about genital warts was obtained from answers to the question, ‘Have you ever had genital warts diagnosed by a doctor, nurse or other health care professional?’ Furthermore, we asked about the age at the first episode of genital warts, the treatment that had been given and episodes in the past 12 months. Information about episodes of other sexually transmitted infections (Chlamydia trachomatis, herpes simples and gonorrhoea) and self-reported circumcision status was also elicited.

    Statistical analysis

    We estimated the overall cumulative incidence of self-reported clinically diagnosed genital warts and the age-specific prevalence in 1-year age groups with 95% CI. Age-specific incidence was estimated on the basis of episodes of genital warts within the past year.

    Associations between various lifestyle factors and self-reported clinically diagnosed genital warts were assessed in multivariate logistic regression models (SAS STAT V.8.2). Associations were measured as ORs with 95% CI. The variables included in the age-adjusted regression model were based on studies reported in the literature and availability in our questionnaire.11–13 ,18 The variables for the mutually adjusted model were selected from among those significant at a 10% level in the age-adjusted models. Variables were retained in the model if they had a significant effect themselves, or if they influenced the other variables in the final model. The continuous variable ‘age’ was initially modelled as linear splines with knots placed according to quartiles in cases. We tested whether the model could be reduced to one with linear associations. As age showed no significant deviation from linearity, it was considered linear in the multivariate models.

    To estimate the age-specific incidence of genital warts, we used age at first diagnosis of genital warts, and the incidence proportion of having had genital warts at a certain age was estimated by the life-table (actuarial) method, stratified according to birth cohort. We compared birth cohorts by log-rank testing.

    Results

    The median age of the men in the survey was 34 years; men aged 18–20 years constituted 8.6% of the study group, and men aged 41–45 years comprised 26.4%. Most of the participants were either married or cohabiting (67%), and 41% had basic schooling of 11 years or more (high school). Current smoking was reported by 31%, and 16% were former smokers. The median lifetime number of sexual partners was 7, with a mean of 12.8, and the mean age at first sexual intercourse was 16.9 years (median, 16 years). Sexually transmitted infections, other than genital warts (Chlamydia trachomatis, herpes simplex or gonorrhoea), were reported by 13%.

    Overall, 1808 men (7.9%; 95% CI 7.6 to 8.2%) reported ever having had a diagnosis of genital warts. The median age at first episode was 22 years, with a mean of 23.3 years. Figure 1 shows the cumulative incidence of self-reported clinically diagnosed genital warts by age. A clear pattern of an increasing cumulative incidence with increasing age was observed. An episode of genital warts was reported by 2.0% (95% CI 1.4 to 2.6%) of the youngest men (18–20 years of age) and by 9.9% (95% CI 9.2 to 10.7%) of men aged 41–45 years.

    Table 1 shows the factors associated with a history of at least one episode of genital warts. Age was strongly correlated, with an increasing risk with increasing age: men aged 41–45 years had an almost three times higher risk than the youngest men, after adjustment (OR 2.9; 95% CI 2.1 to 4.1). Men with a higher education and men who were current, or former smokers, also had increased risks for self-reported genital warts (ever smoker: OR 1.4; 95% CI 1.3 to 1.6).

    View this table:
    Table 1

    Factors associated with self-reported clinically diagnosed genital warts among Danish men aged 18–45 years

    Figure 1
    Figure 1

    Cumulative incidence of self-reported, clinically diagnosed genital warts by age/birth cohort.

    The strongest association with self-reported clinically diagnosed genital warts was the lifetime number of female sexual partners. Men who had had 15 or more sexual partners had an 8.0 times higher adjusted OR for genital warts than those who reported 1–2 sexual partners (95% CI 6.0 to 10.8). Men who reported never having had a female sex partner had a significantly increased risk (OR 2.5; 95% CI 1.5 to 4.1), as did men who had ever had sexual intercourse with a prostitute (OR 1.2; 95% CI 1.0 to 1.4). A history of having had another sexually transmitted infection was significantly associated with genital warts (ever: OR 2.5; 95% CI 2.2 to 2.8; do not remember: OR 3.1; 95% CI 2.1 to 4.5).

    We also assessed the risk for genital warts in relation to circumcision. Men who were circumcised had a decreased risk of borderline significance for genital warts after adjustment (OR 0.8; 95% CI 0.6 to 1.0). Men who were 14 years or younger at first sexual intercourse had a higher risk for genital warts than men who were 15–16 years in the age-adjusted analysis (OR 1.5; significant), but after adjustment for potential confounders the risk was no longer apparent (data not shown).

    Figure 2 shows the occurrence of genital warts in the previous 12 months according to age at enrolment in the study (current age). Of the youngest men (18–20 years of age), about 1% reported at least one episode of genital warts within the past year. Men aged 21–24 years reported the highest occurrence, with 1.83% (95% CI 1.29 to 2.37%) having had genital warts in the past year. In the oldest age group in the study, 0.40% (95% CI 0.24 to 0.56%) reported having had genital warts in the past 12 months.

    Figure 2
    Figure 2

    Proportion of self-reported, clinically diagnosed genital warts in Danish men in the previous 12 months by age.

    We estimated the age-specific incidence proportions of self-reported clinically diagnosed genital warts by age at first diagnosis and by birth cohort, to evaluate whether there were differences in incidence over time for the different birth cohorts (figure 3). In all birth cohorts, there was a rapid increase in the incidence proportion from around 16 years of age up to the mid-20s, whereafter, the increase was marginal. No statistically significant difference was found in the age-specific incidence between birth cohorts (log-rank test, p=0.29).

    Figure 3
    Figure 3

    Estimated cumulative incidence of self-reported clinically diagnosed genital warts in Danish men, by birth cohort.

    Discussion

    In this population-based study of nearly 23 000 Danish men aged 18–45 years, almost 8% reported a history of clinically diagnosed genital warts, ranging from 2% in men aged 18–20 years to nearly 10% among men aged 40–45 years. These cumulative incidences are higher than those found in a study in the USA, where 4% of men aged 18–59 years reported ever having had a diagnosis of genital warts,18 in response to the same question used in our survey. Likewise, a study in Australia found a prevalence of 4% among men in the same age range.12 In a similar study among women in Denmark and three other Nordic countries,11 we found a higher cumulative incidence of self-reported clinically diagnosed genital warts among Danish women aged 18–45 years (10.6%; 95% CI 9.9 to 10.6%) than among the Danish men in the present study (7.9%; 95% CI 7.6 to 8.3%). The study in the USA also showed a higher cumulative incidence among women (7.2%) than men, whereas, the Australian study reported similar prevalences in the two sexes.12

    The social impact of diagnosing and treating genital warts is huge when measured as the economic burden;4 however, genital warts also have a substantial effect at the individual level. Woodhall and colleagues found a negative influence on health-related quality of life,19 with 37% of the participants reporting that having genital warts had significantly affected their quality of life. Therefore, effective strategies to prevent this disease are warranted at the level of both society and the individual.

    In clinical trials to evaluate an HPV vaccine in women against the HPV types that cause most cases of genital warts (types 6 and 11), a significant reduction in incident genital warts was demonstrated.20 ,21 Cases of condyloma were found in none of the vaccinated women and in 48 unvaccinated women, yielding an efficacy of 100% (95% CI 92 to 100%).20 Similar results are emerging in vaccination trials in men.8 The impact of vaccination of women against HPV is beginning to emerge in Australia, where it has been reported that the incidence of genital warts in both women and men dropped significantly after the introduction of mass vaccination of adolescent girls and young women.22 ,23 This raises hope that use of the quadrivalent vaccine in a real-life setting will effectively prevent genital warts.

    In this study, we also estimated the incidence of genital warts, using the number of treatments for genital warts within the past 12 months as a proxy measure. As the answers to this question could potentially also include treatment for recurrent genital warts, the estimated incidence is likely to be a little too high. Nevertheless, the results are in line with those obtained for women in clinical trials of the quadrivalent vaccine. As reported by Garland et al,24 the incidence of genital warts caused by HPV types 6 and 11 was 0.87 per 100 person-years at risk, which is close to the incidence we found of about 1.4% in a similar age group in our study.

    Several factors were associated with self-reported, clinically diagnosed genital warts, including increasing age, ever having smoked, having had other sexually transmitted infections and ever sexual intercourse with a prostitute. These are in line with the findings of other studies and confirm the sexually transmitted nature of this condition.12 ,16 ,18 ,25 Recent studies in both men and women have suggested that smoking is an independent risk factor for incident genital warts.26 ,27 The factor most strongly associated with the risk for genital warts was increasing number of sexual partners; however, men who reported no female sex partners also had a highly significantly increased risk when compared with men reporting one or two female sex partners. Most likely, many of the men who reported no female sex partners were probably homosexuals; the questionnaire specified female partners and did not ask about any male partners.

    Circumcision appeared to offer some protection against genital warts, although the estimate was of only borderline statistical significance. As most penile warts are located on the glans penis and the sulcus coronarius, it is plausible that circumcision might offer protection. In circumcised men, the epithelium in these anatomical locations is cornified in contrast to the uncornified epithelium in uncircumcised men, and the mucosal HPV types 6 and 11 might adhere better to uncornified epithelium. This aspect, and the fact that there is less tissue surface available, have also been suggested by other investigators.28 ,29

    The incidence of a first diagnosis of genital warts at a certain age did not differ by birth cohort in the present study. This is similar to results observed in Danish women, but in contrast with those observed for other Nordic women.11 Especially in Iceland and Norway, the age-specific incidence proportion increased with each subsequent younger birth cohort. The peak age of first episode of genital warts is line with what has been reported in other studies.25 ,30

    One potential limitation of our study is self-reporting of genital warts, which has been questioned as a reliable source for assessing occurrence.31 Obviously, a surveillance system for genital warts, such as that which is in place in the UK, would be the best option. Nevertheless, the question we used to assess genital warts did not ask participants about self-diagnosed episodes, but only about clinically diagnosed genital warts. In addition, in a British survey of sexual behaviour, self-reporting of increasing number of sexual partners correlated well with increasing trends in sexually transmitted infections extracted from external data sources.32 Another limitation is that, despite a high participation rate, we cannot rule out the existence of bias due to non-participation. Nevertheless, the age distribution of participants and non-participants was similar. Furthermore, we previously reported that the distribution of level of schooling and marital status among participants was similar to that in the general Danish population based on data obtained from Statistics Denmark.33

    The strengths of the study are that it is the largest, to date, of the occurrence of genital warts in men. It also has the advantage of being nationwide and based on a random sample of men from the general population. This, taken together with a high participation rate, makes the results potentially more generalisable. Questions about sexual behaviour are not taboo in Denmark, so there were relatively few missing answers to questions related to this issue. Furthermore, the questionnaire also contained questions about several other items and, thus, was not entirely focused on sexual behaviour and sexually transmitted infections.

    In conclusion, the overall cumulative incidence of self-reported clinically diagnosed genital warts in a random sample of Danish men aged 18–45 years was 7.9%, ranging from 2% among the youngest to 10% in the oldest age group. If vaccination against HPV types 6 and 11 becomes widespread, the potential for reducing the burden of genital warts among men is substantial. In Denmark, vaccination with the quadrivalent vaccine has been in place for girls 12 years of age, since January 2009, with the main purpose of preventing cervical cancer and its precursor lesions. It is warranted to monitor the occurrence of genital warts among women as well as men in the coming years as another and more rapidly achievable result of vaccination.

    Key messages

    • A quadrivalent human papillomavirus (HPV) vaccine including HPV types 6, 11, 16 and 18 has been approved for use in men to prevent genital warts and anal cancer

    • Denmark has a national HPV vaccination programme in girls aged 12 years with a coverage of around 80–85%

    • This study shows a cumulative incidence of almost 8% in Danish men aged 18–45 years

    • The study can form the basis for monitoring the effect of vaccination against HPV in men either through herd immunity or directly, if HPV vaccination is offered to men in the future

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    Footnotes

    • Parts of the results of the study were presented at the 24th International Papillomavirus Conference in Beijing, China, November 2007.

    • Contributors CM and SKK designed the study. CM, AN and SKK analysed the data. All authors contributed to the manuscript and approved the final version.

    • Funding This work was supported by Merck and Co, Inc (research grant EPO 8014.023).

    • Competing interests CM has received travel funds for conference participation from Merck and Co, Inc, and Sanofi Pasteur MSD. AN has received travel funds for conference participation from Merck and Co, Inc. K-LL is an employee at Merck Research Laboratories, Merck and Co, Inc. SKK has received consultancy and travel fees from Merck and Co, Inc, and Sanofi Pasteur MSD. She has received funding through her institution to conduct HPV vaccine studies for Merck and Co, Inc, and Sanofi Pasteur MSD.

    • Ethics approval Danish Data Protection Board.

    • Provenance and peer review Not commissioned; externally peer reviewed.