Distribution of human papillomavirus types in anogenital warts of men

doi:10.1016/j.jcv.2008.11.001

Journal of Clinical Virology

Volume 44, Issue 2, February 2009, Pages 111-114

https://doi.org/10.1016/j.jcv.2008.11.001 Get rights and content

Abstract

Background

A wide spectrum of human papillomavirus (HPV) types can infect the male genitalia. An HPV vaccine covering HPV6 and 11 is now available. Detailed data on the distribution of these two types in anogenital warts is needed to assess the potential benefits of the vaccine.

Study design

Anogenital wart specimens collected from 130 Chinese men were examined for HPV-type distribution by a method that covers a broad spectrum of high- and low-risk HPVs, and able to reveal multiple types from a single specimen.

Results

Forty-four (33.8%) of the 130 specimens had a coinfection with multiple HPV types. In 63.1% of cases, only HPV6 and/or HPV11 were/was found. In 26.2% of cases, HPV6 and/or HPV11 were/was found together with one or more other HPV types. In 10.8% of specimens, only non-6/11 HPV types were found. HPV16 and/or 18 were/was found in 12 (9.2%) specimens, with majority (8/12, 66.7%) of which existed as coinfections with HPV6/11. Other HPV types found included HPV39, 51, 52, 55, 59, 61, 62, 68, 58, 72, 81, 83, 84 and CP6108.

Conclusions

A substantial proportion of HPV6/11-positive male anogenital warts are coinfected with other HPV types. The efficacy of HPV6/11 vaccine for preventing these lesions needs to be defined before the benefits of vaccinating men can be precisely assessed.

Introduction

There are about 200 different genotypes of human papillomaviruses, with ∼40 of which can establish infection in the anogenital area. These anogenital HPVs are associated with a wide spectrum of diseases including carcinoma of the cervix, vagina, vulva, anal and penile areas; and benign proliferative lesions referred to as anogenital warts.1, 2, 3 In contrast to the wealth of knowledge on HPV-associated diseases for females, relatively little information is available for males.4, 5

Currently two prophylactic vaccines are available for the prevention of HPV infection. Cervarix™ (GlaxoSmithKline) is a bivalent vaccine containing HPV16 and 18.6, 7 Gardasil™ (Merck Sharp and Dohme) is a quadrivalent vaccine containing HPV6, 11, 16 and 18.8, 9 While these vaccines primarily aim at preventing cervical cancers caused by the high-risk types (HPV16 and 18), the inclusion of low-risk types (HPV6 and 11) in Gardasil™ provides an additional benefit for preventing anogenital warts.

It is well documented that HPV16 and 18 accounts for 70–80% of cervical cancers worldwide,¹⁰ but the precise proportion of genital warts being caused by HPV6 and 11 is less clear. It has been shown that there are geographical variations in high-risk HPV types found in cervical intraepithelial neoplasia.10, 11 In particular, two high-risk types HPV52 and HPV58 are overrepresented in Southeast Asia¹² including the current study site Hong Kong.13, 14, 15 Information on the distribution of low-risk HPV types in anogenital warts in this region is still lacking. Whether the geographical variation in HPV-type distribution also occurs in anogenital warts is not known.

This study examined the distribution of HPV types in anogenital warts of a cohort of Chinese men in Hong Kong to contribute essential data for assessing the potential benefits of HPV vaccines that contain HPV6 and 11.

Section snippets

Patient recruitment and sample collection

Patient recruitment was conducted from July to September 2006 at a Government-funded public male social hygiene clinic which provides free-of-charge service for patients with sexually transmitted diseases. Consecutive patients with a clinical diagnosis of anogenital wart were invited to participate with an informed consent. The study was approved by the Institutional Ethics Committee.

A cervical rambrush (Jiangsu Suyun Medical Materials Co. Ltd., China) was used to collect cells from the surface

Results

Of the 180 recruited patients, 135 had a brush sample showing positive results for beta-globin PCR, and hence regarded as having an adequate specimen quality for HPV detection. Altogether 130 samples, each from a different patient, were tested positive for HPV DNA. The 5 samples that were positive for beta-globin PCR but negative for HPV DNA might contain HPV DNA below the detection limit of our PCR, and were excluded from the following type distribution analyses. The age of these 130 male

Discussion

Genital wart is one of the most common sexually transmitted diseases with an annual prevalence of about 1% among the sexually active population in the USA²⁰; and a retrospective study in England and Wales has reported an almost fourfold increase in clinical attendance from 1971 to 1994.²¹

Studies based on subclinical surveillance samples of the male anogenital area have detected a variety of HPV types, for instance HPV6, HPV53, HPV84 and HPV16²² were most commonly found from a cohort in Tucson,

Conflict of interest

None to declare.

References (28)

J.M. Partridge et al.
Genital human papillomavirus infection in men
Lancet Infect Dis
(2006)
D.M. Harper et al.
Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial
Lancet
(2006)
J. Paavonen et al.
Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial
Lancet
(2007)
A.T. Newall et al.
Cost-effectiveness analyses of human papillomavirus vaccination
Lancet Infect Dis
(2007)
M. Stanley
Prevention strategies against the human papillomavirus: the effectiveness of vaccination
Gynecol Oncol
(2007)
F.T. Cutts et al.
Human papillomavirus and HPV vaccines: a review
Bull World Health Organ
(2007)
J.M. Palefsky
HPV infection in men
Dis Markers
(2007)
H. zur Hausen
Papillomaviruses and cancer: from basic studies to clinical application
Nat Rev Cancer
(2002)
E.F. Dunne et al.
Prevalence of HPV infection among men: a systematic review of the literature
J Infect Dis
(2006)
FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl...

S.M. Garland et al.

Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases

N Engl J Med

(2007)

J.S. Smith et al.

Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update

Int J Cancer

(2007)

G.M. Clifford et al.

Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis

Br J Cancer

(2003)

Y.P. Bao et al.

Human papillomavirus type-distribution in the cervix of Chinese women: a meta-analysis

Int J STD AIDS

(2008)

Cited by (60)

Evaluation of human papillomavirus DNA detection-guided aminolaevulinic acid-mediated photodynamic therapy for the treatment of condyloma acuminata
2019, Photodiagnosis and Photodynamic Therapy
Aminolaevulinic acid-mediated photodynamic therapy (ALA-PDT) is used to treat condyloma acuminata (CA), yielding a high clearance rate and low recurrence rate. Consecutive human papillomavirus (HPV) DNA detection can be used to dynamically monitor the therapeutic efficiency of PDT. Here, we evaluated the efficacy of ALA-PDT in the context of different HPV infection states.
One hundred thirty-eight patients with HPV infection and visible anogenital warts were enrolled. Microwave or radiofrequency was used to remove visible lesions before PDT. HPV DNA detection was performed using real-time polymerase chain reaction before each PDT session and at follow-up. Treatment was halted after the patient showed two negative results for HPV DNA detection in a row.
Of the 138 patients enrolled in the study, 72 completed treatment. Multisite HPV-infected patients required more sessions of PDT than did single-site infected patients to reach the endpoint of treatment. Compared with patients with only external CA, individuals with internal CA required more sessions to eliminate HPV infection. The total number of PDT sessions performed in the multitype HPV-infected group was significantly higher than that in the single-type infected group. Patients with non-high-risk (HR)-HPV infection required fewer PDT sessions than did those with HR-HPV infection by the end of treatment. Sixty-nine patients were followed-up for at least 6 months, only 2.9% of whom showed recurrence.
Combined ALA-PDT and HPV DNA detection was an effective strategy for the treatment of CA. Patients with multisite and multitype HPV infection required more PDT sessions to eliminate the virus.
HPV-related external genital lesions among men residing in Brazil
2017, Brazilian Journal of Infectious Diseases
Citation Excerpt :
In the current study HPV DNA was detected in 87.3% of condyloma biopsies, in line with previous results of 91% HPV prevalence in condyloma samples of women enrolled in the placebo arm of a vaccine trial.19 HPV-6 and HPV-11 were the most prevalent viral types detected in condylomas in agreement with previous reports,20–23 although HPV-6 detection surpassed that of HPV-11 (48.1% versus 36.7%) in these samples. About 16% of HPV-6 and HPV-11 infections progressed to a condyloma with the same viral type during follow-up; however median time to progression was higher among HPV-6 positive men (nine months for HPV-6 versus 6.8 months for HPV-11).
The aims of this study were to determine the incidence of external genital lesions (EGLs), specifically histologically confirmed condyloma (genital warts) and Penile Intraepithelial Neoplasia (PeIN), and genital HPV infection progression to EGLs among healthy men aged 18–73 residing in Brazil. Subjects included 1118 men enrolled in the HPV Infection in Men (HIM) study between July 2005 and June 2009. At each visit, EGLs were biopsied and subjected to pathological evaluation. HPV status in genital swabs and biopsies was determined by Linear Array and INNO-LiPA, respectively. Age-specific EGLs incidence and the proportion and median time to EGL development were estimated. Kaplan–Meier cumulative incidence rates at 6, 12, and 24 months were determined. During follow-up, 73 men developed an incident EGL. Men could develop multiple EGLs and there were 36 men with condyloma, 27 men with lesions suggestive of condyloma, six men with PeIN, and 20 men with non-HPV lesions. HPV-positive men who developed EGLs were younger (p = 0.002) than men that did not develop lesions. Among the 815 men with HPV infection, 4% progressed to EGL with the same HPV detected in the swab. During follow up, 15.7% of genital HPV-6 and HPV-11 infections progressed to condyloma (median progression time of nine months for HPV-6 versus 6.8 months for HPV-11). Approximately 1% of HPV-16 infections progressed to PeIN with a median progression time of 25 months. HPV types covered by the 4-valent HPV vaccine were detected in 82.3% and 83.3% of condyloma and PeIN, respectively. The high burden of HPV and high frequency of progression to disease underscores the need to offer HPV prophylactic vaccination to men to reduce the overall burden of infection and diseases caused by HPV.
Infections of the Genital Tract: Human Papillomavirus–Related Infections
2017, European Urology, Supplements
Citation Excerpt :
About 20–30% of genital warts will spontaneously regress; however, recurrence of warts is common [74]. More than 90% of genital warts are caused by nononcogenic HPV types 6 and 11 [75], but approximately one-third of genital warts have multiple HPV types including coinfection with oncogenic types [76]. Data available for the HPV type distribution of genital warts in men are sparse.
The human papillomaviruses (HPVs) are a major global health burden, playing a part in diseases ranging from genital warts to malignancies such as penile cancer in men and cervical cancer in women.
To explore the molecular biology and epidemiology of HPV infection; the diseases linked to it; and current prevention strategies, including the potential role of vaccination.
The relevant papers, reviews, and guidelines pertaining to the topics were collected for the purpose of this review from PubMed and online guidelines resources including the European Association of Urology and the Centers for Disease Control and Prevention.
The current knowledge on genital HPV in men is explained and summarised.
There is an urgent need for more data on the incidence and persistence of HPV at the different anatomic sites, the incidence of external genital lesions, and the types of HPV in these lesions. This will allow a more comprehensive understanding of the natural history of HPV infection and its progression to both benign and malignant disease in men and will help formulate the development and implementation of vaccination programs.
This review explores the molecular biology and epidemiology of human papillomavirus (HPV) infection; the diseases linked to it; and current prevention strategies, including the potential role of vaccination. There is an urgent need for more data on the incidence and persistence of HPV at the different anatomic sites, the incidence of external genital lesions, and the types of HPV in these lesions.
Immune status does not predict high-risk HPV in anal condyloma
2016, Journal of Surgical Research
Citation Excerpt :
In multivariate analysis, we did not find that immune status was a significant predictor of dysplasia or hrHPV, although hrHPV was significantly and independently associated with development of dysplasia. Although some studies have shown increased prevalence of hrHPV subtypes in the HIV+ and IC populations compared with NIC [4,9], more recent studies have shown a higher than expected prevalence of hrHPV subtypes in immunocompetent populations [10–14]. For example, Ball et al. [11] examined HPV types in 31 immunocompetent patients and found that 48% of the population had infection with at least one type of hrHPV.
More than 90% of anal condyloma is attributed to nonhigh risk strains of human papillomavirus (HPV), thus patients with anal condyloma do not necessarily undergo HPV serotyping unless they are immunocompromised (IC). We hypothesized that IC patients with anal condyloma have a higher risk of high-risk HPV and dysplasia than nonimmunocompromised (NIC) patients.
We performed a retrospective chart review of patients who underwent surgical treatment by a single surgeon for anal condyloma from 1/2000 to 1/2012. HPV serotyping was performed on all patient samples. We compared incidence of high-risk HPV and dysplasia in condyloma specimens from IC and NIC patients.
High-risk HPV was identified in 14 specimens with serotypes 16, 18, 31, 33, 51, 52, and 67. Twenty-two cases (18.3%) had dysplasia. Invasive carcinoma was identified in one IC patient. The prevalence of dysplasia or high-risk HPV was not significantly different between IC and NIC groups. High-risk HPV was a significant independent predictor of dysplasia (odds ratio [OR] = 5.2; 95% CI = 1.24–21.62). Immune status, however, was not a significant predictor of high-risk HPV (OR = 1.11; 95% CI = 0.16–5.12) nor dysplasia (OR = 0.27; 95% CI = 0.037–1.17).
IC patients did not have a significantly higher prevalence or risk of high-risk HPV or dysplasia in our study. HPV typing of all condylomata, regardless of immune status, should be considered as it may help predict risk of neoplastic transformation or identify NIC patients with an increased risk of developing anal intraepithelial neoplasia.
Prevalence and risk factors of anal human papillomavirus infection among men with anal condyloma acuminata by HIV status in ShenZhen, Southeast China: A retrospective cohort study
2023, Journal of Medical Virology
Epidemiology of human papillomavirus on condyloma acuminatum in Shandong Province，China
2023, Human Vaccines and Immunotherapeutics

View all citing articles on Scopus

^☆: Part of the results was presented in the 24th International Papillomavirus Conference, 3–9 November 2007. Abstract No. PS8-01.

View full text

Distribution of human papillomavirus types in anogenital warts of men☆

Abstract

Background

Study design

Results

Conclusions

Introduction

Section snippets

Patient recruitment and sample collection

Results

Discussion

Conflict of interest

Lancet Infect Dis

Lancet

Lancet

Lancet Infect Dis

Gynecol Oncol

Human papillomavirus and HPV vaccines: a review

Bull World Health Organ

HPV infection in men

Dis Markers

Papillomaviruses and cancer: from basic studies to clinical application

Nat Rev Cancer

Prevalence of HPV infection among men: a systematic review of the literature

J Infect Dis

Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases

N Engl J Med

Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update

Int J Cancer

Comparison of HPV type distribution in high-grade cervical lesions and cervical cancer: a meta-analysis

Br J Cancer

Human papillomavirus type-distribution in the cervix of Chinese women: a meta-analysis

Int J STD AIDS