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Prevalence of HPV Infection among Men: A Systematic Review of the Literature
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The Journal of Infectious Diseases Oct 15, 2006;194:1044-1057
References included below.
Eileen F. Dunne,1 Carrie M. Nielson,3 Katherine M. Stone,2 Lauri E. Markowitz,1 and Anna R. Giuliano4
1Division of STD Prevention, US Centers for Disease Control and Prevention, and 2Consultant practice, Atlanta, Georgia; 3Arizona Cancer Center, University of Arizona, Tucson; 4Department of Interdisciplinary Oncology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, Florida
ABSTRACT
Background. Human papillomavirus (HPV) infection is estimated to be the most common sexually transmitted infection; an estimated 6.2 million persons are newly infected every year in the United States. There are limited data on HPV infection in heterosexual men.
Methods. We conducted a systematic review of the literature by searching MEDLINE using the terms "human papillomavirus," "HPV," "male," "seroprevalence," and "serology" to retrieve articles published from 1 January 1990 to 1 February 2006. We included studies that had data on population characteristics and that evaluated male genital anatomic sites or specimens for HPV DNA or included assessments of seropositivity to HPV type 6, 11, 16, or 18 in men. We excluded studies that had been conducted only in children or immunocompromised persons (HIV infected, transplant recipients, or elderly).
Results. We included a total of 40 publications on HPV DNA detection and risk factors for HPV in men; 27 evaluated multiple anatomic sites or specimens, 10 evaluated a single site or specimen, and 3 evaluated risk factors or optimal anatomic sites/specimens for HPV detection. Twelve studies assessed site- or specimen-specific HPV DNA detection. HPV prevalence in men was 1.3%-72.9% in studies in which multiple anatomic sites or specimens were evaluated; 15 (56%) of these studies reported >20% HPV prevalence. HPV prevalence varied on the basis of sampling, processing methods, and the anatomic site(s) or specimen(s) sampled. We included 15 publications reporting HPV seroprevalence. Rates of seropositivity depended on the population, HPV type, and methods used. In 9 studies that evaluated both men and women, all but 1 demonstrated that HPV seroprevalence was lower in men than in women.
Conclusion. HPV infection is highly prevalent in sexually active men and can be detected by use of a variety of specimens and methods. There have been few natural-history studies and no transmission studies of HPV in men. The information that we have reviewed may be useful for future natural-history studies and for modeling the potential impact of a prophylactic HPV vaccine.
Human papillomaviruses (HPVs) are members of the Papillomaviridae family of DNA viruses. More than 100 types have been identified; about 40 types infect the anogenital region. Anogenital HPV types have been further classified into low-risk types (e.g., 6 and 11), which are associated with anogenital warts and mild dysplasia, and high-risk types (e.g., 16, 18, 31, and 45), which are associated with high-grade dysplasia and anogenital cancers, such as cervical and anal carcinoma. Anogenital HPV infections are the most common sexually transmitted infection; an estimated 6.2 million persons are newly infected every year in the United States [1, 2]. Most infections are asymptomatic or subclinical and become undetectable over time.
\Most research has focused on HPV infection in women because of the association between HPV infection and cervical cancer; however, information on HPV infection and serologic responses to infection in men is informative for evaluations of the potential impact of prophylactic HPV vaccines [3, 4]. We review studies of asymptomatic anogenital HPV infections in men and the seroprevalence of HPV types 6, 11, 16, and 18.
METHODS
We conducted a systematic review of the literature by searching MEDLINE for articles published in English from 1 January 1990 through 1 February 2006. We also included references from the retrieved publications. We excluded studies conducted only in children <12 years old or immunosuppressed persons (HIV infected, transplant recipients, or elderly) and studies that included <20 men. When possible, we included results only for asymptomatic men.
To retrieve publications reporting HPV DNA prevalence, we used the search terms "HPV," "human papillomavirus," and "male." We included studies that used polymerase chain reaction or hybrid capture to detect HPV DNA from genital anatomic sites or specimens. We excluded publications that evaluated only prostate, anal, or testicular samples.
To retrieve publications reporting HPV seropositivity, we used the same search terms but also included "serology" and "seroprevalence." We included studies that evaluated IgG antibodies to HPV-6, -11, -16, and -18 virus-like particles (VLPs) or to L1 or L2 peptides.
RESULTS
HPV DNA detection studies. Our search identified 148 eligible studies; review of these studies resulted in the inclusion of 43 publications. Three studies had information reported in another publication and were excluded, resulting in a total of 40 studies [5-44]. Two studies had information on risk factors only [43, 44], and 1 study had information on anatomic sites and samples [42].
Study populations included a variety of age and racial/ethnic groups in diverse geographic locations. Twenty-seven studies evaluated multiple anatomic sites and specimens (table 1) [6-9, 11-13, 16, 19, 22, 23, 25-28, 30-41], and 10 studies evaluated single sites or specimens (table 2) [5, 10, 14, 15, 17, 18, 20, 21, 24, 29]. Twelve studies evaluated multiple sites or specimens and reported the results for each site or specimen separately (table 3) [11, 12, 22, 23, 25, 30-33, 35, 36, 42]. Four longitudinal studies evaluated the incidence and/or persistence of HPV (table 4) [19, 31, 34, 41].
HPV prevalence in men was 1.3%-72.9% in studies in which multiple anatomic sites or specimens were evaluated; 15 (56%) of these studies reported an overall HPV prevalence 20% (table 1). HPV prevalence varied both within and among populations (figure 1).
Sampling methods. Sampling methods varied among studies. Most sampling methods involved rubbing or rotating a swab or brush, either dry or moist, on the genital epithelium. One study that evaluated 3 different sampling techniques (10 men for each method) found that using a saline-wetted sterile Dacron swab after having rubbed the sampling site with a small piece of emery paper was superior for specimen adequacy to using the swab alone or using a saline-wetted sterile cytobrush [32]. One study found that self-collection yielded a greater proportion of adequate specimens than physician-collected specimens [36].
Sites of detection. The prevalence of HPV varied on the basis of sampling, processing methods and the anatomic site(s) or specimen(s) sampled. Twelve studies compared HPV detection in individual anatomic sites or specimens (table 3). Most studies evaluated the glans, corona, prepuce, or shaft of the penis. Although no 2 studies included all the same sites, 8 sampled the corona and/or glans, and the reported HPV prevalence was 6.5%-50% [11, 22, 23, 30-33, 36]. Three studies evaluated the penile shaft, and the reported HPV prevalence was 5.6%-51.5% [11, 32, 36]. Four studies sampled the prepuce, and the reported HPV prevalence was 24.0%-50.0% [23, 32, 33, 36]. HPV prevalence was 7.1%-46.2% in 5 studies that evaluated the scrotum [11, 23, 32, 36, 42]. Seven studies evaluated the distal 1-3 cm of the urethra, and the reported HPV prevalence was 8.7%-50% [12, 22, 23, 31, 33, 35, 42]. The few studies that evaluated the perianal area, anus, or rectum found an HPV prevalence of 0%-32.8% [11, 23, 30, 31]. Semen was evaluated in 2 studies that compared multiple anatomic sites and specimens [25, 35] and in 7 studies that evaluated semen as a single specimen [5, 15, 17, 20, 21, 24, 29]; HPV was detected in 2.2%-41.3% of men evaluated and in up to 82.9% of specimens. Most studies that evaluated urine reported an HPV prevalence of <7% [11, 12, 22, 25, 32, 35]. Seven studies reported sample adequacy by the evaluation of -globin [11, 12, 22, 32, 35, 36, 42]. Samples collected from the prepuce, shaft, glans, corona, and scrotum were the most likely to have adequate DNA; 70%-98.5% were -globin positive.
HPV DNA types. The most common anogenital HPV types detected in men varied by study but were similar to the types commonly detected in women. Type 16 was consistently among the most common; however, other types were also reported (types 6, 11, 18, 31, 33, 42, 52, 53, 54, 59, and 84) [7, 9, 27, 39, 41]. One study found that undetermined types may be found more frequently in men than in women [39]. Multiple types were commonly found in men; 51.1% of men with HPV in one study had multiple HPV types detected [41].
Risk factors for HPV DNA detection. Ten studies evaluated the risk factors associated with HPV infection in men in a cross-sectional analysis [6, 9, 13, 22, 26, 27, 30, 41, 43, 44]; of these, 5 reported factors statistically significantly associated with infection. Few studies included multivariate analyses to evaluate factors independently associated with HPV infection [27, 43]. Two studies included multivariate analysis to evaluate the factors independently associated with the acquisition or persistence of HPV infection [19, 41].
Measures of sexual behavior were associated with HPV infection in men. Five cross-sectional studies found risk factors related to sexual behavior, including young age at first sexual intercourse [9]; a greater number of regular, lifetime, and recent sex partners [13, 27, 44]; and a greater number of sex partners before and during marriage [9, 44]. In addition, female sex partners' lifetime number of sex partners [44] and a high frequency of sexual intercourse [43] were associated with HPV detection. However, only 2 of these studies included a multivariate analysis that adjusted for confounding [27, 43]. Longitudinal studies found that anal intercourse with men [41] and having had 3 sex partners [19] were independently associated with HPV acquisition.
The effect of condom use was evaluated in 5 cross-sectional analyses [13, 30, 41, 43, 44], 1 of which found, after controlling for confounding factors, a significant reduction in the risk of HPV infection in men who used condoms consistently [43]. Consistent condom use during the preceding 3 months was associated with a decreased risk of both any and high-risk HPV infection; condom use during the last occurrence of anal sex was associated in the same study with a decreased risk of low-risk HPV infection [43]. Another study demonstrated that condom use significantly reduced the risk of HPV in circumcised men but not in uncircumcised men [44]. One longitudinal study found that consistent or occasional condom use was independently associated with a reduced risk of acquiring HPV [19].
The effect of circumcision was evaluated in 5 cross-sectional studies [26, 27, 41, 43, 44], 3 of which found, after adjusting for confounding factors, that circumcision was associated with a statistically significant lower risk of HPV infection [27, 41, 43]. The statistically significant reduction in risk ranged from 20% to 48%. One longitudinal study found that self-reported circumcision was independently associated with a reduced risk of HPV persistence [19].
Two cross-sectional studies evaluated factors associated with the detection of high-risk versus low-risk HPV types [27, 43]; only 1 adjusted for confounding factors [43]. Factors associated with high-risk HPV types were young age [27], a higher lifetime number of sex partners [27], and higher frequency of sexual intercourse [43]. High-risk HPV types were less likely to be detected in circumcised men or in those who had used condoms consistently during the preceding 3 months [43]. Factors associated with the detection of low-risk HPV types were young age [27], a history of genital warts [27], the presence of genital warts [43], and the number of sex partners during the preceding year [27]. Low-risk HPV types were less likely to be detected in circumcised men and in those who had used condoms during their last occurrence of anal sex [43]. Two longitudinal studies found that the detection of >1 HPV type at baseline was independently associated with HPV persistence [19, 41].
Natural-history studies. Only 4 studies prospectively evaluated HPV infection in men [19, 31, 34, 41] (table 4). The duration of follow-up varied among studies. Of men who tested negative for HPV at baseline, between 13.8% and 22.7% acquired HPV (i.e., tested positive during follow-up). Independent predictors of HPV acquisition were anal sex with other men (adjusted odds ratio [AOR], 5.34 [95% confidence interval {CI}, 1.18-24.2]) [41] and having had 3 sex partners since the last clinic visit (AOR, 17.2 [95% CI, 4.6-64.7]) [19]. Factors independently associated with a reduced risk of HPV acquisition were consistent or occasional condom use (AOR, 0.2 [95% CI, 0.1-0.8]) [19] and high socioeconomic status (AOR, 0.28 [95% CI, 0.12-0.64]) [41].
The definition of persistence varied by study; persistence occurred in 6%-11% of men in the study or in 50%-57.5% of men with HPV infection at the baseline visit. Factors associated with persistence included multiple HPV types detected at the baseline visit and circumcision [19, 41].
Transmission studies. Few studies have evaluated HPV infection in both men and their female sex partners; all of these studies published to date have evaluated cross-sectional concordance [6, 23, 37, 39]. A recent cross-sectional study of heterosexual couples found that 37% of partners were infected with the same HPV type. Notable findings were that overall viral loads were much lower in penile-scrape specimens than in cervical-scrape specimens. Higher loads of HPV-16 were associated with having a partner who was also positive for HPV-16 [39]. Another study that assessed HPV by DNA detection or peniscopy found that 76% of male sex partners of women with HPV were HPV DNA positive; that study did not evaluate type-specific concordance [23]. A study of 50 couples found that HPV type-specific concordance between sex partners was more common than predicted by chance (P = .01) [6]. Another study found that only 22.7% of couples had the same HPV type in genital specimens [37].
To our knowledge, there have been no longitudinal transmission studies; however, recent modeling efforts seeking to match transmission characteristics to available incidence and prevalence data estimated the median probability per sex act of HPV transmission to be about 40% (range, 5%-100%) [45].
HPV seroprevalence studies. We identified 42 studies of HPV seroprevalence; 14 met our inclusion criteria (table 5) [46-59]. Eleven publications evaluated HPV-16 seroprevalence [46, 49-55, 57-59]; 5 evaluated HPV-6 seroprevalence [47, 49, 51, 55, 56]; 4 evaluated HPV-11 seroprevalence [48, 51, 55, 56]; and 1 evaluated HPV-18 seroprevalence [59]. One study used a combined assay for HPV-6 and -11 seroprevalence [51]. Nine studies compared HPV seroprevalence in men and women [46-48, 51-53, 57-59].
HPV-16 seropositivity differed by study population; most studies in sexually transmitted disease (STD) clinics reported a higher rate of seropositivity than studies in other populations. The range of reported seropositivity in male STD clinic attendees was between 18.7% [58] and 48% [49] in the United States. The seropositivity to HPV-16 in males in the general population was 7.9% in the United States [57]. HPV-16 seropositivity was similar in male STD clinic attendees in Denmark, Greenland, and Jamaica [52, 53]; however, a lower seroprevalence was noted in China, and a higher seroprevalence was noted in Sweden [54, 55]. Eight of 9 studies that compared seroprevalence in men and women reported a higher seroprevalence in women than in men [46, 48, 51-53, 57-59].
Comparisons of studies of HPV-6, -11, and -18 seropositivity were more difficult, because most studies of HPV-6 and -11 were conducted in STD clinic attendees, and the study of HPV-18 was conducted in clinics or community centers. HPV-6 or -11 seroprevalence ranged from 26.4% [51] to 41% [49] in one study. The estimate of HPV-18 seroprevalence in one study was 18.8% [59].
Risk factors for HPV seropositivity. Six studies reported factors associated with HPV seropositivity [49, 51-53, 57, 58], and all included multivariate analyses to identify factors independently associated with HPV seropositivity. All studies evaluated HPV-16 seropositivity as an outcome; one also evaluated HPV-6 and -11 seropositivity [51], and another evaluated HPV-6 seropositivity [49].
Age was evaluated in 6 studies [49, 51-53, 57, 58]. In 3 studies, age (generally, being >20 years old) was associated with an increased likelihood of detection of HPV-16 antibodies [51, 52, 58]. No association was observed between age and HPV-6 and -11 seropositivity in the 2 studies that evaluated age as a risk factor [49, 51].
Sexual behavior was evaluated in 6 studies [49, 51-53, 57, 58] and was found to be independently associated with HPV seropositivity, including the lifetime [53] and recent [49, 51, 52, 58] number of sex partners. Having had >1 occasional sex partner within the preceding year was associated with an increased risk of HPV seropositivity in 1 study [58]. Younger age (<18 years) at first sexual intercourse was evaluated in 2 studies [53, 57] and was a significant risk factor in 1 study [53]. One study found an increased risk of HPV-16 seropositivity in men who had had sex with a man [57].
Three studies, 2 of which included multivariate analyses, evaluated condom use and HPV seropositivity [51, 52, 58]. One study found that HPV-16 seropositivity was more likely to occur with less-frequent condom use during the preceding year (never vs. more than one-half the time) [52]. One study examined consistent condom use in a bivariate analysis and found no significant association between condom use and the detection of HPV-16 or -6 and -11 antibodies [51].
DISCUSSION
HPV infection is common in sexually active men and can be detected by use of a variety of specimens and methods. HPV in asymptomatic men is frequently associated with various measures of sexual activity. Few studies are available that have determined the frequency of acquisition and the duration of infection in men.
Our review demonstrates a wide range of HPV DNA prevalence among men, depending on the study population and the type and number of anatomic sites evaluated. Most studies in men found prevalences as high as those reported in studies in women. Our review identified HPV prevalence in men as high as 72.9% and usually >20%; HPV prevalence in women in one systematic review was 14%-90% [60].
The best anatomic sites for sampling in men-taking into consideration convenience of sampling, adequacy of the sample, and detection of HPV DNA-appear to be the glans, corona, prepuce, and shaft of the penis. It is possible that combined samples from these sites may be optimal. Sampling from these sites appears to have several advantages: samples are consistently adequate, and sample collection is simple and painless. Scrotum samples are often adequate, but, in most studies, they were less likely to yield HPV DNA. The prepuce, when present, is possibly the best single site for HPV DNA detection.
Specimens that are less useful include urine, semen, and urethral swabs. The source of infection in these specimens is unclear, but it could be the urethra, seminal fluid, sperm, or vas deferens. Semen and urethral specimens often have adequate beta-globin and HPV DNA but are difficult and sometimes uncomfortable to collect. beta-globin and HPV DNA detection is often poor from urine specimens, although these specimens could be the easiest to obtain.
The sites on the penis that consistently yield HPV-the glans, corona, prepuce, and most of the shaft-are covered when a condom is properly used. However, it is clear that other areas, such as the scrotum and inguinal area, may also harbor HPV; despite consistent and correct condom use, these areas would not be protected or covered by a condom. Although it was less common than at other sites, 7.1%-46.2% of men had HPV detected on the scrotum or inguinal area.
Factors associated with HPV infection and seropositivity in men varied across studies; however, the most consistent findings were associations with sexual behavior. The potential value of circumcision in preventing HPV infection is unclear. Most cross-sectional studies and 1 longitudinal study demonstrated a lower risk of HPV infection associated with circumcision. One study demonstrated significant differences between circumcised and uncircumcised men that could have resulted in confounding [44]; not all studies take into consideration characteristics of the population such as sexual behaviors and cultural differences when evaluating this characteristic. An ongoing randomized controlled clinical trial measuring the effect of circumcision on the prevention of HPV will address some questions regarding the value of circumcision for the prevention of HPV.
Serologic testing for IgG antibodies to HPV may be a better measurement of cumulative exposure; antibodies may indicate past infection in persons who have no history or current signs of HPV disease. Previous evaluations of serologic testing in women demonstrated that serologic testing likely underestimates the cumulative incidence of HPV infection [61]. We found that HPV seroprevalence varied depending on the population evaluated. The detection of HPV antibodies may be more common in persons with disease such as anogenital warts, but not all men with these clinical findings have antibodies to HPV infection, and many never develop an immune response. The higher HPV seroprevalence in men with a history of anogenital warts, compared with men who have warts at the time of sampling, is attributed to the time it takes to develop an immune response to HPV [55, 56].
A higher seroprevalence of HPV types 6, 11, 16, and 18 has been found in women than in men. Possible explanations may be related to the sites of infection in men, compared with those in women; the vigor of the serologic response to genital infection; or other host genetic and immunologic factors.
Our evaluation of HPV DNA prevalence has several limitations. First, the methods for examining HPV DNA varied among studies, including methods of sampling, HPV DNA detection, analysis, and the reporting of results. Second, not all studies evaluated the adequacy of the sample, which might influence HPV DNA detection. HPV DNA is detectable in the absence of adequate beta-globin, but the significance of this finding is unclear [62].
Our evaluation of serologic studies also has several limitations. Methods varied among studies, including methods to determine cutoffs for positivity, the quantitation of antibodies to VLPs, and the reporting of results. Cross-reactivity has been observed between HPV types 6 and 11; among types 16, 31, 33, and 58; and among types 18, 39, 45, and 59 [63]. In addition to cross-reactivity, which limits the specificity of findings, there is no standard method to establish ELISA absorbance cutoff values for positivity. A common method for establishing a cutoff value is to calculate the mean absorbance value and add 2 or 3 SDs; however, it is not clear whether the mean should be determined from all subjects [53, 64], control subjects [54], virgin women [47, 49], or children [51]. Karem et al. [65] recommended the use of multiple control groups (children and adults) to obtain cutoff values applicable to the general population. In addition, few publications reported the sensitivity and specificity of their tests; when results were reported, they varied considerably. In one study, 93% sensitivity and 98.5% specificity was reported for an HPV-16 assay [57]; by contrast, another study demonstrated 50.6% sensitivity and 90% specificity [46].
Many questions exist regarding the clinical utility of testing men for HPV infection; there is no current indication for testing men. At present, there is a Food and Drug Administration (FDA)-approved HPV test that is indicated for women in the setting of the screening and management of cervical cancer [66, 67]. Screening for HPV infection is not recommended for men for many reasons: infection is very common, no FDA-approved test is available, and finding HPV infection does not indicate an increased risk of disease or cancer in men or their sex partners. In addition, no therapy has been identified that eradicates infection. The evaluation and treatment of male sex partners of women with clinical or subclinical infection (genital warts or abnormal Pap smear results) is also not known to have a benefit [68, 69].
The present review of HPV infection and seroprevalence in men will be useful for the design of natural-history studies and the measurement of transmission. Future research will inform models designed to estimate the impact of various prevention strategies, including prophylactic HPV vaccines.
References
1. Cates W Jr, American Social Health Association. Estimates of the incidence and prevalence of sexually transmitted diseases in the United States. Panel. Sex Transm Dis 1999; 26(Suppl 1):S2-7. First citation in article PubMed
2. Weinstock H, Berman S, Cates W Jr. Sexually transmitted diseases among American youth: incidence and prevalence estimates, 2000. Perspect Sex Reprod Health 2004; 36:6-10. First citation in article PubMed CrossRef
3. Villa LL, Costa RL, Petta CA, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 2005; 6:271-8. First citation in article PubMed CrossRef
4. Harper DM, Franco EL, Wheeler C, et al. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. GlaxoSmithKline HPV Vaccine Study Group. Lancet 2004; 364:1757-65. First citation in article PubMed CrossRef
5. Aynaud O, Poveda JD, Huynh B, Guillemotonia A, Barrasso R. Frequency of herpes simplex virus, cytomegalovirus and human papillomavirus DNA in semen. Int J STD AIDS 2002; 13:547-50. First citation in article PubMed CrossRef
6. Baken LA, Koutsky LA, Kuypers J, et al. Genital human papillomavirus infection among male and female sex partners: prevalence and type-specific concordance. J Infect Dis 1995; 171:429-32. First citation in article PubMed
7. Baldwin SB, Wallace DR, Papenfuss MR, et al. Human papillomavirus infection in men attending a sexually transmitted disease clinic. J Infect Dis 2003; 187:1064-70. First citation in article Full Text PubMed
8. Bleeker MC, Hogewoning CJ, Van Den Brule AJ, et al. Penile lesions and human papillomavirus in male sexual partners of women with cervical intraepithelial neoplasia. J Am Acad Dermatol 2002; 47:351-7. First citation in article PubMed CrossRef
9. Castellsague X, Ghaffari A, Daniel RW, Bosch FX, Munoz N, Shah KV. Prevalence of penile human papillomavirus DNA in husbands of women with and without cervical neoplasia: a study in Spain and Colombia. J Infect Dis 1997; 176:353-61. First citation in article PubMed
10. Della Torre G, Donghi R, de Campos Lima PO, et al. Human papillomavirus genomes in male urethral cells. Am J Pathol 1992; 141:1181-6. First citation in article PubMed
11. Fife KH, Coplan PM, Jansen KU, et al. Poor sensitivity of polymerase chain reaction assays of genital skin swabs and urine to detect HPV 6 and 11 DNA in men. Sex Transm Dis 2003; 30:246-8. First citation in article PubMed
12. Forslund O, Hansson BG, Rymark P, Bjerre B. Human papillomavirus DNA in urine samples compared with that in simultaneously collected urethra and cervix samples. J Clin Microbiol 1993; 31:1975-9. First citation in article PubMed
13. Franceschi S, Castellsague X, Dal Maso L, et al. Prevalence and determinants of human papillomavirus genital infection in men. Br J Cancer 2002; 86:705-11. First citation in article PubMed CrossRef
14. Geddy PM, Wells M, Lacey CJ. Lack of detection of human papillomavirus DNA in male urine samples. Genitourin Med 1993; 69:276-9. First citation in article PubMed
15. Green J, Monteiro E, Bolton VN, Sanders P, Gibson PE. Detection of human papillomavirus DNA by PCR in semen from patients with and without penile warts. Genitourin Med 1991; 67:207-10. First citation in article PubMed
16. Hippelainen M, Syrjanen S, Hippelainen M, et al. Prevalence and risk factors of genital human papillomavirus (HPV) infections in healthy males: a study on Finnish conscripts. Sex Transm Dis 1993; 20:321-8. First citation in article PubMed
17. Inoue M, Nakazawa A, Fujita M, Tanizawa O. Human papillomavirus (HPV) type 16 in semen of partners of women with HPV infection. Lancet 1992; 339:1114-5. First citation in article PubMed CrossRef
18. Kataoka A, Claesson U, Hansson BG, Eriksson M, Lindh E. Human papillomavirus infection of the male diagnosed by Southern-blot hybridization and polymerase chain reaction: comparison between urethra samples and penile biopsy samples. J Med Virol 1991; 33:159-64. First citation in article PubMed
19. Kjaer SK, Munk C, Winther JF, Jorgensen HO, Meijer CJ, van den Brule AJ. Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 2005; 14:1528-33. First citation in article PubMed CrossRef
20. Kyo S, Inoue M, Koyama M, et al. Detection of high-risk human papillomavirus in the cervix and semen of sex partners. J Infect Dis 1994; 170:682-5. First citation in article PubMed
21. Lai YM, Lee JF, Huang HY, et al. The effect of human papillomavirus infection on sperm cell motility. Fertil Steril 1997; 67:1152-5. First citation in article PubMed CrossRef
22. Lazcano-Ponce E, Herrero R, Munoz N, et al. High prevalence of human papillomavirus infection in Mexican males: comparative study of penile-urethral swabs and urine samples. Sex Transm Dis 2001; 28:277-80. First citation in article PubMed CrossRef
23. Nicolau SM, Camargo CG, Stavale JN, et al. Human papillomavirus DNA detection in male sexual partners of women with genital human papillomavirus infection. Urology 2005; 65:251-5. First citation in article PubMed CrossRef
24. Olatunbosun O, Deneer H, Pierson R. Human papillomavirus DNA detection in sperm using polymerase chain reaction. Obstet Gynecol 2001; 97:357-60. First citation in article PubMed CrossRef
25. Rintala MAM, Pollanen PP, Nikkanen VP, Grenman SE, Syrjanen SM. Human papillomavirus DNA is found in the vas deferens. J Infect Dis 2002; 185:1664-7. First citation in article Full Text PubMed
26. Shin H-R, Franceschi S, Vaccarella S, et al. Prevalence and determinants of genital infection with papillomavirus, in female and male university students in Busan, South Korea. J Infect Dis 2004; 190:468-76. First citation in article Full Text PubMed
27. Svare EI, Kjaer SK, Worm AM, Osterlind A, Meijer CJ, van den Brule AJ. Risk factors for genital HPV DNA in men resemble those found in women: a study of male attendees at a Danish STD clinic. Sex Transm Infect 2002; 78:215-8. First citation in article PubMed CrossRef
28. Takahashi S, Shimizu T, Takeyama K, et al. Detection of human papillomavirus DNA on the external genitalia of healthy men and male patients with urethritis. Sex Transm Dis 2003; 30:629-33. First citation in article PubMed
29. Tanaka H, Karube A, Kodama H, Fukuda J, Tanaka T. Mass screening for human papillomavirus type 16 infection in infertile couples. J Reprod Med 2000; 45:907-11. First citation in article PubMed
30. van der Snoek EM, Niesters HG, Mulder PG, van Doornum GJ, Osterhaus AD, van der Meijden WI. Human papillomavirus infection in men who have sex with men participating in a Dutch gay-cohort study. Sex Transm Dis 2003; 30:639-44. First citation in article PubMed
31. Van Doornum GJ, Prins M, Juffermans LH, et al. Regional distribution and incidence of human papillomavirus infections among heterosexual men and women with multiple sexual partners: a prospective study. Genitourin Med 1994; 70:240-6. First citation in article PubMed
32. Weaver BA, Feng Q, Holmes KK, et al. Evaluation of genital sites and sampling techniques for detection of human papillomavirus DNA in men. J Infect Dis 2004; 189:677-85. First citation in article Full Text PubMed
33. Wikstrom A, Lidbrink P, Johansson B, von Krogh G. Penile human papillomavirus carriage among men attending Swedish STD clinics. Int J STD AIDS 1991; 2:105-9. First citation in article PubMed
34. Wikstrom A, Popescu C, Forslund O. Asymptomatic penile HPV infection: a prospective study. Int J STD AIDS 2000; 11:80-4. First citation in article PubMed CrossRef
35. Astori G, Pipan C, Muffato G, Botta GA. Detection of HPV-DNA in semen, urine and urethral samples by dot blot and PCR. New Microbiol 1995; 18:143-9. First citation in article PubMed
36. Hernandez BY, McDuffie K, Goodman MT, et al. Comparison of physician- and self-collected genital specimens for detection of human papillomavirus in men. J Clin Microbiol 2006; 44:513-17. First citation in article PubMed CrossRef
37. Hippelainen MI, Yliskoski M, Syrjanen S, et al. Low concordance of genital human papillomavirus (HPV) lesions and viral types in HPV-infected women and their male sexual partners. Sex Transm Dis 1994; 21:76-82. First citation in article PubMed
38. Takahashi S, Takeyama K, Miyamoto S, et al. Incidence of sexually transmitted infections in asymptomatic healthy young Japanese men. J Infect Chemother 2005; 21:76-82. First citation in article PubMed
39. Bleeker MCG, Hogewoning CJA, Berkhof J, et al. Concordance of specific human papillomavirus types in sex partners is more prevalent than would be expected by chance and is associated with increased viral loads. Clin Infect Dis 2005; 41:612-20. First citation in article Full Text PubMed
40. Rosenblatt C, Lucon AM, Pereyra EA, Pinotti JA, Arap S, Ruiz CA. HPV prevalence among partners of women with cervical intraepithelial neoplasia. Int J Gynaecol Obstet 2004; 84:156-61. First citation in article PubMed CrossRef
41. Lajous M, Mueller N, Cruz-Valdez A, Aguilar LV, Franceschi S, Hernandez-Avila M. Determinants of prevalence, acquisition, and persistence of human papillomavirus in healthy Mexican military men. Cancer Epidemiol Biomarkers Prev 2005; 14:1710-6. First citation in article PubMed CrossRef
42. Aguilar LV, Lazcano-Ponce E, Vaccarella S, et al. Human papillomavirus in men: comparison of different genital sites. Sex Transm Infect 2006; 82:31-3. First citation in article PubMed CrossRef
43. Baldwin SB, Wallace DR, Papenfuss MR, Abrahamsen M, Vaught LC, Giuliano AR. Condom use and other factors affecting penile human papillomavirus detection in men attending a sexually transmitted disease clinic. Sex Transm Dis 2004; 31:601-7. First citation in article PubMed
44. Castellsague X, Bosch FX, Munoz N, et al. Male circumcision, penile human papillomavirus infection, and cervical cancer in female partners. N Engl J Med 2002; 346:1105-12. First citation in article PubMed CrossRef
45. Burchell AN, Richardson H, Mahmud SM, et al. Modeling the sexual transmissibility of human papillomavirus infection using stochastic computer simulation and empirical data from a cohort study of young women in Montreal, Canada. Am J Epidemiol 2006; 163:534-43. First citation in article PubMed CrossRef
46. Carter JJ, Madeline MM, Shera K, et al. Human papillomavirus 16 and 18 L1 serology compared across anogenital cancer sites. Cancer Res 2001; 61:1934-40. First citation in article PubMed
47. Carter JJ, Wipf GC, Hagensee ME, et al. Use of human papillomavirus type 6 capsids to detect antibodies in people with genital warts. J Infect Dis 1995; 172:11-8. First citation in article PubMed
48. Eisemann C, Fisher SG, Gross G, Muller M, Gissmann L. Antibodies to human papillomavirus type 11 virus-like particles in sera of patients with genital warts and in control groups. J Gen Virol 1996; 77:1799-803. First citation in article PubMed
49. Hagensee ME, Kiviat N, Critchlow CW, et al. Seroprevalence of human papillomavirus types 6 and 16 capsid antibodies in homosexual men. J Infect Dis 1997; 176:625-31. First citation in article PubMed
50. Hisada M, Rabkin CS, Strickler HD, Wright WE, Christianson RE, van den Berg BJ. Human papillomavirus antibody and risk of prostate cancer. JAMA 2000; 283:340-1. First citation in article PubMed CrossRef
51. Slavinsky J III, Kissinger P, Burger L, Boley A, DiCarlo RP, Hagensee ME. Seroepidemiology of low and high oncogenic risk types of human papillomavirus in a predominantly male cohort of STD clinic patients. Int J STD AIDS 2001; 12:516-23. First citation in article PubMed CrossRef
52. Strickler HD, Kirk GD, Figueroa JP, et al. HPV 16 antibody prevalence in Jamaica and the United States reflects differences in cervical cancer rates. Int J Cancer 1999; 80:339-44. First citation in article PubMed CrossRef
53. Svare EI, Kjaer SK, Nonnenmacher B, et al. Seroreactivity to human papillomavirus type 16 virus-like particles is lower in high-risk men than in high-risk women. J Infect Dis 1997; 176:876-83. First citation in article PubMed
54. Wideroff L, Schiffman M, Hubbert N, et al. Serum antibodies to HPV 16 virus-like particles are not associated with penile cancer in Chinese males. Viral Immunol 1996; 9:23-5. First citation in article PubMed
55. Wikstrom A, Eklund C, Von Krogh G, Lidbrink P, Dillner J. Levels of immunoglobulin G antibodies against defined epitopes of the L1 and L2 capsid proteins of human papillomavirus type 6 are elevated in men with a history of condylomata acuminata. J Clin Microbiol 1992; 30:1795-800. First citation in article PubMed
56. Wikstrom A, Eklund C, von Krogh G, Lidbrink P, Dillner J. Antibodies against human papillomavirus type 6 capsids are elevated in men with previous condylomas. APMIS 1997; 105:884-8. First citation in article PubMed
57. Stone KM, Karem KL, Sternberg MR, et al. Seroprevalence of human papillomavirus type 16 infection in the United States. J Infect Dis 2002; 186:1396-402. First citation in article Full Text PubMed
58. Thompson DL, Douglas JM Jr, Foster M, et al. Seroepidemiology of infection with human papillomavirus 16, in men and women attending sexually transmitted disease clinics in the United States. J Infect Dis 2004; 190:1563-74. First citation in article Full Text PubMed
59. Kreimer AR, Alberg AJ, Viscidi R, Gillison ML. Gender differences in sexual biomarkers and behaviors associated with human papillomavirus-16, -18, and -33 seroprevalence. Sex Transm Dis 2004; 31:247-56. First citation in article PubMed
60. Revzina NV, Diclemente RJ. Prevalence and incidence of human papillomavirus infection in women in the USA: a systematic review. Int J STD AIDS 2005; 16:528-37. First citation in article PubMed CrossRef
61. Carter JJ, Koutsky LA, Hughes JP, et al. Comparison of human papillomavirus types 16, 18, and 6 capsid antibody responses following incident infection. J Infect Dis 2000; 181:1911-9. First citation in article Full Text PubMed
62. Kruger Kjaer S, Munk C, Winther JF, et al. Acquisition and persistence of human papillomavirus infection in younger men: a prospective follow-up study among Danish soldiers. Cancer Epidemiol Biomarkers Prev 2005; 14:1528-33. First citation in article PubMed CrossRef
63. Coursaget P. Serology for human papillomavirus. Salud Publica Mex 2003; 45(Suppl 3):S361-6. First citation in article PubMed
64. Hamsikova E, Ludvikova V, Smahel M, Sapp M, Vonka V. Prevalence of antibodies to human papillomaviruses in the general population of the Czech Republic. Int J Cancer 1998; 77:689-94. First citation in article PubMed CrossRef
65. Karem KL, Poon AC, Bierl C, Nisenbaum R, Unger E. Optimization of a human papillomavirus-specific enzyme-linked immunosorbent assay. Clin Diagn Lab Immunol 2002; 9:577-82. First citation in article PubMed CrossRef
66. Wright TC, Shiffman M, Solomon D, et al. Interim guidance for the use of human papillomavirus DNA testing as an adjunct to cervical cytology for screening. Obstet Gynecol 2004; 103:304-9. First citation in article PubMed
67. Saslow D, Runowicz CD, Solomon D, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 2002; 52:342-62. First citation in article PubMed
68. Krebs HB, Helmkamp BF. Does the treatment of genital condylomata in men decrease the treatment failure rate of cervical dysplasia in the female sexual partner? Obstet Gynecol 1990; 76:660-3. First citation in article PubMed
69. Krebs HB, Helmkamp BF. Treatment failure of genital condylomata acuminata in women: role of the male sexual partner. Am J Obstet Gynecol 1991; 165:337-40. First citation in article PubMed
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