Detection of human papillomavirus infection in penile samples through liquid-based cytology and polymerase chain reaction.
ABSTRACT The human papillomavirus (HPV) is strongly related to cervical cancer and its precursor lesions. However, unlike in the case of women, there are limited data regarding HPV infection in men. Analysis of male HPV infection is frequently hindered by the lack of consistency in collection methods, sample adequacy, and low sensitivity of cytologic analysis.
The objective of the current study was to compare the results of liquid-based cytology and HPV DNA testing through polymerase chain reaction in 99 penile samples collected from men presenting with condyloma acuminate or male partners of HPV-infected women who had attended a public health service in the city of Belo Horizonte, Minas Gerais, Brazil. Classic and nonclassic cytomorphologic signs were adopted to evaluate the presence of HPV infections in penile smears.
HPV DNA was detected in 93 (93.9%) of the 99 samples analyzed. Koilocytosis was detected in 1 smear and nonclassic signs were detected in 23 smears, 22 of which were found to be positive for HPV DNA.
The cytopathologic detection of HPV infection in penile samples collected for liquid-based cytology is low, even when cytologic nonclassic signs are applied, and does not appear to improve the diagnosis of HPV infection in men.
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ABSTRACT: OBJECTIVE: To determine the incidence of dysplasia as a preneoplastic change and high-risk human papilloma virus (HPV) infection in penile condylomas, which are common HPV-related lesions and considered a risk factor for penile cancer. METHODS: Histologic analysis was done of 58 consecutive penile condylomas with tissue diagnosis. An immunohistochemical panel that included stains for p53, Ki-67, and p16(INK4a) was also used. HPV typing was successfully performed in 43 lesions. Genotyping was accomplished through polymerase chain reaction and flow-through hybridization with an HPV GenoArray Diagnostic Test kit. RESULTS: Dysplasia was observed in 13 of the 58 condylomas (22%). High-risk HPV DNA was detected in 5 of 10 dysplastic lesions (50%) for which tissue blocks were available for study. High-risk HPV was not detected in the nondysplastic lesions (P <.001). Ki-67 ≥20% above the basal layer of epithelium and p53-positive immunostaining occurred more frequently in dysplastic lesions than in nondysplastic lesions; however, the difference was not statistically significance. Staining for p16(INK4a) was not helpful. CONCLUSION: Anogenital condylomas in men are usually treated using destructive methods or with medication. We suggest that at least a part of the lesion must be removed and sent for histopathologic examination. If the histologic result shows significant dysplastic alteration, the lesion should be further investigated to determine the subtype of infective virus, because 50% of such lesions are associated with high-risk HPV. When oncogenic pathogens are found, careful patient follow-up for recurrences and counseling for the patient and his sexual partner(s) may be warranted.Urology 11/2012; · 2.13 Impact Factor
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ABSTRACT: Objective: To investigate the prevalence of genital high-risk human papillomavirus (HR-HPV) in male sexual partners of HR-HPV infected women and the concordance of viral types in couples in China, and comprehend the role of men play in HPV transmission to women. Methods/Materials: 94 asymptomatic women and their husbands from rural Chaozhou participated in epidemiologic screening for HPV infection. Cervical cells from females were collected for high risk HPV screening by real time-PCR, and they were positive for at least 1 of 13 HR-HPV subtypes, then these samples were genotyped. Approximately one mouth later, penile epithelial cells from 94 asymptomatic husbands were collected for HPV genotyping. At the same time, a cross-sectional study was conducted in 366 male patients from sexually transmitted disease (STD) outpatient clinic in China for the prevalence of genital HR-HPV infection in men having frequent sex behavior. Penial epithelial cells were collected for HPV 6/11 and HPV 16/18 detection by fluorescent real-time quantified PCR. Results: Among 94 couples, the prevalence of genital HR-HPV infection in men whose wife was positive for cervical HR-HPV was 5.32% (5/94). Only 2.63% (2/76) had the same high risk viral type presented by their wife. HPV 16 proved to be the most prevalent viral type in men and in couples. Of 366 male patients from STD outpatient clinic, the prevalence of HPV 16/18 infection in men with or without HPV 6/11 was 6.85% and 8.16%, respectively. The incidence of HPV 16/18 was higher in men aged more than 35 years than the young men (18-35 years). Conclusion: The prevalence of genital HR-HPV infection in male sexual partners of HPV-positive women in China was lower than that expected, and the concordance of high risk viral type between couples was extremely low. These data suggested that infected men consitute an important viral reservoir, contributing to transmission of HR-HPV to women and maintenance of infection, but HR-HPV infection may be less likely to persist in men than in women.Asian Pacific journal of cancer prevention: APJCP 03/2013; 14(3):1755-60. · 1.50 Impact Factor
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ABSTRACT: OBJECTIVE: To investigate the prevalence of high-risk (HR) and low-risk (LR) human papillomavirus (HPV) in prepuces of boys and men without any HPV related lesions. PATIENTS AND METHODS: Between 2009 and 2011, a total collective of 250 boys and men were investigated in this prospective study. The samples were subdivided into 3 groups regarding their age, consisting of 125 (50 %) children (0-10 years), 38 (15.2 %) adolescents (11-20 years) and 87 (34.8 %) adults (>20 years). In situ hybridization (ISH) was performed to detect HR and LR virus types within the epithelium, followed by microscopic interpretation and determination between episomal and integrative signal pattern. RESULTS: Our results revealed high levels of HPV concentration (HR and LR) in all age groups: HR versus LR positivity was seen in 45.5 versus 35 % (children), 60.6 versus 63.6 % (adolescents) and 58.3 versus 48.6 % (adults). The topmost rate of HR (59.8 %)- and LR (50.6 %)-positive probes was found in the group with high estimated sexual activity (>14 years). CONCLUSION: Concerning the high prevalence of male HPV infection even in children, indicating non-sexual transmission pathways, inclusion of boys in the vaccination program seems to be required reducing their burden of HPV related disease.World Journal of Urology 12/2012; 31(6). · 3.42 Impact Factor
Detection of Human Papillomavirus Infection in Penile
Samples Through Liquid-based Cytology and
Polymerase Chain Reaction
Maria Gabrielle de Lima Rocha, MSc1
Fa ´bio Lopes Faria, BSc1
Maria do Carmo M. Souza, BSc2
Annamaria Ravara Vago, PhD3
Ana Paula Fernandes, PhD1
Paula A´vila Fernandes, MD, PhD1
1Department of Clinical and Toxicology Analyses,
Federal University of Minas Gerais, Belo Hori-
zonte, Minas Gerais, Brazil.
2Polyclinic of Medical Attendance of the Region
Center-South, Training Center in Sexually Trans-
missible Illnesses of the District South Center of
the City Hall of Belo Horizonte, Minas Gerais,
3Department of Morphology, Institute of Biologi-
cal Sciences, Federal University of Minas Gerais,
Belo Horizonte, Minas Gerais, Brazil.
BACKGROUND. The human papillomavirus (HPV) is strongly related to cervical
cancer and its precursor lesions. However, unlike in the case of women, there are
limited data regarding HPV infection in men. Analysis of male HPV infection is
frequently hindered by the lack of consistency in collection methods, sample ad-
equacy, and low sensitivity of cytologic analysis.
METHODS. The objective of the current study was to compare the results of
liquid-based cytology and HPV DNA testing through polymerase chain reaction
in 99 penile samples collected from men presenting with condyloma acuminate
or male partners of HPV-infected women who had attended a public health ser-
vice in the city of Belo Horizonte, Minas Gerais, Brazil. Classic and nonclassic
cytomorphologic signs were adopted to evaluate the presence of HPV infections
in penile smears.
RESULTS. HPV DNA was detected in 93 (93.9%) of the 99 samples analyzed. Koi-
locytosis was detected in 1 smear and nonclassic signs were detected in 23
smears, 22 of which were found to be positive for HPV DNA.
CONCLUSIONS. The cytopathologic detection of HPV infection in penile samples
collected for liquid-based cytology is low, even when cytologic nonclassic signs are
applied, and does not appear to improve the diagnosis of HPV infection in men.
Cancer (Cancer Cytopathol) 2008;114:489–93. ? 2008 American Cancer Society.
KEYWORDS: human papillomavirus, cytology, polymerase chain reaction, penile.
regarding HPV infections in women, little is known concerning this
infection in men, which complicates our understanding of the epi-
demiologic and clinical aspects of HPV infection in this segment of
the population. Because of its high prevalence and high rate of
infection, the dissemination of HPV occurs frequently among sexu-
ally active individuals and men may be considered significant disse-
minators of this infection among women.1,2
The diagnosis of HPV infection in men is frequently achieved by
means of a biopsy, which is only performed when a lesion is sus-
pected and/or the female partner has been diagnosed with HPV
infection. Thus, HPV infection is not as routinely diagnosed in men
as it is in women.
In men, the cytologic changes that suggest HPV infection are
similar to those noted in women (ie, koilocytosis, dyskeratocytosis,
and nuclear changes).3However, a low frequency of koilocytosis
(4%-5% of the samples) is actually found in penile smears,4-6
uman papillomavirus (HPV) is strongly related to cervical can-
cer and its precursor lesions. In contrast to the wealth of data
Funded by Fundac ¸a? o de Amparo ? a Pesquisa do
Estado de Minas Gerais (FAPEMIG) and Canselao
Nacional de Desenvolvimento Cientifico e Tec-
nol? ogico (CNPq) (grant no. CDS 206 of 04 and
48034 of 04-2).
Address for reprints: Paula?Avila Fernandes, MD,
PhD, Department of Clinical and Toxicology Anal-
yses, Faculty of Pharmacy, Federal University of
Minas Gerais, Av. Antˆ onio Carlos, 6627-CEP
31270 901 Brazil; Fax: (011) 55 31 34096985;
Received April 30, 2008; revision received July
10, 2008; accepted July 14, 2008.
ª2008 by the American Cancer Society
Published online 30 October 2008 in Wiley InterScience (www.interscience.wiley.com).
thereby hampering the diagnosis of HPV infection by
means of cytologic methods. Nicolau et al6,7reported
that koilocytosis was detected in 4.7% of distal ure-
thral samples and in 1.6% of those collected at the
corona of the glans and the internal surface of the
prepuce, compared with 13.5% as detected in biopsy
specimens. In addition, the small number of cells in
penile smears, and the low adherence of these cells
to the slide, make cytologic analysis quite difficult.
Moreover, the atypical changes are discrete.3
Schneider et al8observed that the sensitivity of
the cytologic diagnosis of HPV infections in cervical
samples might be improved by the application of a
panel of 9 cytologic nonclassic signs: mild koilocyto-
sis, mild dyskeratocytosis, cleared cytoplasm, kerato-
hyalin granules, condensation of filaments, spindle
cells, nuclear hyperchromatism, binucleation or mul-
tinucleation, and perinuclear halos. Mild koilocytosis,
mild dyskeratocytosis, hyperchromatic nuclei, binu-
cleation or multinucleation, and cleared cytoplasm
demonstrated the most significant statistical correla-
tion with HPV infection. When these 5 signs were
combined according to their validity, discriminant
analysis could identify 84% of the HPV-positive cases
and 92% of the HPV-negative smears correctly,
thereby improving the sensitivity of the cytologic
Although still controversial, liquid-based cytol-
reported to increase the sensitivity of cervical cytol-
ogy and the proportion of slides that are satisfactory
for assessment. In addition, liquid-based cytology
also offers the possibility of performing a molecular
To our knowledge to date, there are still scant
data in the literature regarding both the accuracy of
liquid-based cytology as well as the application of
cytologic nonclassic signs to detect HPV infection in
penile samples. For this reason, herein we performed
a comparison of the results of liquid-based cytology
(applying classic and nonclassic signs) and HPV DNA
testing through polymerase chain reaction (PCR) in
penile samples from men presenting with condyloma
acuminate or who were sexual partners of women
who were diagnosed with HPV infection.
MATERIALS AND METHODS
A total of 99 male patients attending a public health
clinic for sexually transmitted diseases in the city of
Belo Horizonte, Minas Gerais, Brazil participated in
the current study. The men were attending the clinic
for either the diagnosis and treatment of condyloma
acuminate (n 5 58 men) or because their sexual
partners had been diagnosed with an HPV infection
(n 5 41 men). Information concerning the research
was provided to all the participants, and all signed a
free and informed consent form approved by the
institutional ethics committee of the Federal Univer-
sity of Minas Gerais.
The penile samples were collected for liquid-based
cytology using the DNA Citoliq system (Digene, Va-
lencia, Calif). Material was brushed from the glans
and the internal surface of the prepuce, including
the sulcus and the corona, and placed in transport
tubes. Cells were then suspended in a preservative
liquid, which allowed them to be used for both
liquid-based cytology and DNA extraction.
The molecular analysis was performed in DNA
extracted from collected samples using proteinase K
and isopropanol DNA precipitation.11All samples
were submitted to PCR using the oligonucleotides
PC03/PC04, which amplifies a 120 pairs of basis (bp)
sequence of a human b-globulin gene12so as to cre-
ate an internal control with which to verify the integ-
rity and quality of the DNA extracted. The GP51/
GP61 oligonucleotides13were used to detect HPV
DNA. Positive samples, previously tested for HPV
infection, were included in each set of reactions as
positive controls. Each sample was tested in tripli-
cate, and negative samples were tested in different
DNA concentrations to confirm the results. PCR reac-
tions were prepared with 0.05 mM each of dNTP
(GIBCO BRL, Gaithersburg, MD), 1 U of Taq poly-
merase (Phoneutria, MG, Brazil), 1.5 mM of MgCl2,
and the specific oligonucleotides in a final volume of
10.0 lL. PCR reactions were performed in MJ PT100
thermocyclers (MJ Research, Waltham, Mass). PCR
reactions consisted of 35 cycles of 1 minute at 948C
for denaturing, 1 minute at 558C for annealing, and 1
minute at 728C for extension to amplify the human
b-globulin gene fragment. For the amplification of
HPV DNA, a ‘‘touch-down’’ PCR condition was used,
which consisted of 5 initial cycles of 1 minute at
958C, 1 minute at 458C, and 1 minute at 728C, fol-
lowed by 35 cycles of 1 minute at 958, 1 minute at
458C, and 1 minute at 728C.
The penile smears were prepared using the DNA
Citoliq system (Digene) and stained by the Papanico-
laou method. The smears were screened for the pre-
sence of the classic cytomorphologic signs of HPV
490CANCER (CANCER CYTOPATHOLOGY)December 25, 2008 / Volume 114 / Number 6
infection: koilocytosis and dyskeratocytosis. In addi-
tion, 9 nonclassic cytologic signs described previously
in cervical samples8were also examined as follows:
mild koilocytosis, mild dyskeratocytosis, cleared cyto-
plasm, keratohyalin granules, condensation of fila-
binucleation or multinucleation, and perinuclear
The smears were analyzed randomly without
previous knowledge of the molecular findings.
HPV DNA was detected in 93 (93. 9%) of the 99 sam-
ples analyzed. Of the 99 smears evaluated, only 1
demonstrated koilocytosis. With regard to the pre-
sence of cytologic nonclassic signs of HPV infection,
23 (23.2%) smears displayed at least 1 of the nonclas-
sic signs, and the presence of more than 1 sign
was frequently observed (Table 1). The correlation
between the presence of cytologic nonclassic signs
and HPV DNA is shown in Table 2.
Among the 23 smears, which demonstrated cyto-
logic nonclassic signs, only 1 was found to be nega-
tive for HPV DNA. No correlation was found between
the number of nonclassic signs observed and the
presence of HPV DNA. The number of signs in each
smear was variable and, even in samples demon-
strating only 1 nonclassic sign, the presence of HPV
DNA was detected. Finally, the distribution of cytolo-
gic nonclassic signs of HPV infection among patients
with condyloma acuminate and the partners of
women diagnosed with HPV infection proved to be
The medical records of 83 of the 99 patients who
had participated in the current study were reviewed
after a period of 1 year had elapsed after the collec-
tion of the penile samples. None of the patients had
presented with clinical or histopathologic evidence of
high-grade squamous intraepithelial lesions or penile
carcinoma. The recurrence of condyloma acuminate
was evaluated. Thirteen of 58 patients (22.4%) with
condyloma acuminate developed recurrence of the
lesion within this period. All 6 HPV DNA-negative
patients did not present with clinical evidence of or
have positive biopsies for HPV infection.
A high rate of HPV infection was detected (93%) in
the current study. The detection of HPV DNA in men
may vary significantly depending on the study popu-
lation and the presence of detectable lesions, as well
as the type and number of anatomic sites evaluated.
Higher detection rates are usually reported in sam-
ples collected at the glans, corona, prepuce, and
shaft of the penis compared with the scrotum, by
urethral swabs, and in urine and semen. In addition,
sampling from these areas produces more consistent
results and is simple and painless. However, it
appears that collection at multiple sites may increase
sensitivity.2Thus, the high prevalence of HPV DNA
observed in the current study may be attributed not
only to the population analyzed (ie, men presenting
with condyloma acuminate and as partners of HPV-
positive females) but also to sampling at multiple
Among the 99 penile smears, only 1 demon-
strated koilocytosis. There is also a wide variation
(5%-81%) reported among different studies regarding
the detection of HPV infection by cytologic analysis
of penile samples, including urethral sampling.4,14-18
This variation is most likely because of differences in
the site of sample collection, the presence of penile
and/or urethral lesions identified macroscopically or
by peniscopy, and, even more commonly, because of
the cytologic criteria adopted by authors to identify
the cytologic changes attributed to HPV infection.
Frequency of Cytologic Nonclassic Signs of HPV Infection in
Cytologic Nonclassic Signs No. of Smears (%)*
Binucleation or multinucleation
Condensation of filaments
Smears without any nonclassic sign
HPV indicates human papillomavirus.
*The presence of more than 1 sign was frequently observed in each smear.
Correlation Between the Presence of Cytologic Nonclassic Signs of
HPV Infection and the Detection of HPV DNA Through PCR in
Positive No. (%)
Negative No. (%)
HPV indicates human papillomavirus; PCR, polymerase chain reaction.
*Smears containing koilocytosis and nonclassic signs were not considered in this analysis.
Penile Cytology and HPV Infection/de Lima Rocha et al 491
Koilocytosis is not always considered as a necessary
cellular change for the diagnosis of HPV infection in
penile smears. Aynaud et al17reported that cellular
changes suggesting HPV infection were present in
81% of men with urethral lesions, but also in 15% of
men without lesions. It is worth noting that these
authors considered the presence of binucleation or
multinucleation, a larger nucleus, hyperchromatic
nucleus, and thicker nuclear membrane, among
others, to be indicative of HPV infection, but did not
include koilocytosis. However, such features may
represent a reactive atypia and may lead to false-
positive results, as also reported by Aynaud et al.17
Considering only those studies that applied simi-
lar methodology and criteria (penile smears and the
presence of koilocytosis as being indicative of HPV
infection), the results listed herein are in agreement
with those reported by others4-6suggesting that the
detection of HPV infection by means of penile cytol-
ogy is low (1.6%-5% of the cases).
Liquid-based cytology has been compared with
conventional cytology in the screening of cervical
cancer. It has been reported that this procedure
allows for a reduction of 3.2% and 9.3% in false-neg-
ative results in patients with CIN3 and CIN2, respec-
tively, provided both have been confirmed through
biopsies.19Moreover, the detection of atypical squa-
mous cells of undetermined significance, low–grade
squamous intraepithelial lesions, or more severe
lesions is higher when applying this method, result-
ing in a more precise diagnosis of the precursor
lesions of cervical cancer.20Results from a recent
meta-analysis,10including studies aimed at compar-
ing conventional cytology with liquid-based cytology
using biopsy results as a gold standard, suggested
that liquid-based cytology is more sensitive, but not
necessarily more specific, than conventional cytol-
In the current study, the results obtained using
liquid-based cytology in penile samples from men
with condyloma acuminate or who were partners of
HPV-infected women, with a consequent high pro-
bability of presenting with an HPV infection, were
compared with those obtained by the molecular
detection of HPV infection. However, even applying
liquid-based cytology, an increased sensitivity in HPV
detection was not observed, in keeping with the data
available in the literature regarding conventional
The cytologic nonclassic signs were also ana-
lyzed to evaluate whether their detection would
improve the diagnosis of HPV infection in penile
samples. Of the 23 samples that demonstrated at
least 1 nonclassic sign, 22 were found to be positive
for HPV DNA. When considering all the HPV DNA–
positive samples, applying cytologic nonclassic signs
permitted the identification of HPV infections in 24%
(22 of 92 cases) of the cases. Although the applica-
tion of nonclassic signs represented an improvement
(24% vs 1%) in the sensitivity of the cytologic diagno-
sis, it remained very low. It is worth noting that sam-
ples with a variable number of cytologic nonclassic
signs (range, 1-5 signs) were considered in this analy-
sis, although it may be assumed that the presence of
only 1 nonclassic sign is not sufficient to suggest
HPV infection in penile samples, especially because
some of these signs can also be observed in reactive
and inflammatory processes. However, because the
cytologic findings associated with HPV infection in
penile cytology are not as well investigated as they
are in cervical cytology, it is possible that more
subtle changes, regarded as unspecific in cervical cy-
tology, would be required for the diagnosis of HPV
infections in penile cytology. The evaluation of the
presence of these signs in HPV DNA–negative penile
samples may help to determine whether they are in
fact quantitatively and qualitatively associated with
HPV infection in men. The low frequency of HPV
DNA–negative samples could be considered to be a
limitation of the current study; additional studies will
be required to clarify this issue.
In conclusion, the detection of HPV infection in
penile samples through liquid-based cytology, even
after the application of cytologic nonclassic signs,
was found to be low (24%) in the current study, and
does not appear to constitute an adequate method
for the detection of HPV infection in men.
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Penile Cytology and HPV Infection/de Lima Rocha et al 493