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1679
Squamous Papilloma of the Urinary Tract Is Unrelated
to Condyloma Acuminata
Liang Cheng, M.D.1,2
Bradley C. Leibovich, M.D.3
John C. Cheville, M.D.4
Dharamdas M. Ramnani, M.D.4
Thomas J. Sebo, M.D.4
Ajay Nehra, M.D.3
Reza S. Malek, M.D.3
Horst Zincke, M.D., Ph.D.3
David G. Bostwick, M.D.3,4
1
Department of Pathology, Indiana University
School of Medicine, Indianapolis, Indiana.
2
Department of Urology, Indiana University School
of Medicine, Indianapolis, Indiana.
3
Department of Urology, Mayo Clinic, Rochester,
Minnesota.
4
Department of Pathology, Mayo Clinic, Rochester, Minnesota.
BACKGROUND. To the authors’ knowledge, there is no previous report of squamous
papilloma of the urinary tract. It is uncertain whether there is a correlation
between squamous papilloma, condyloma acuminatum, and verrucous carcinoma.
METHODS. The authors evaluated the clinical and pathologic features of squamous
papilloma (5 of the bladder, 2 of the urethra), condyloma acuminatum (3 cases),
and verrucous carcinoma (3 cases) of the urinary bladder and performed human
papillomavirus (HPV) DNA in situ hybridization studies to determine whether HPV
was a common feature shared by these lesions. In addition, DNA ploidy evaluation
by image cytometry and p53 immunohistochemical staining were performed.
RESULTS. Squamous papilloma of the urinary tract occurred in elderly women and
followed a benign clinical course with infrequent recurrence. All squamous papillomas were HPV DNA negative and DNA diploid with no or minimal p53 nuclear
accumulation. Condyloma acuminata of the bladder contained HPV DNA, increased p53 protein expression, and aneuploid DNA content. All three cases of
condyloma acuminata were associated with coexistent condylomata of the external
genitalia, and two required pelvic exenteration for uncontrolled expansile growth.
Verrucous carcinoma of the bladder occurred in elderly patients. All three cases of
verrucous carcinoma were negative for HPV DNA and DNA aneuploid, and they
exhibited consistent p53 expression.
CONCLUSIONS. These data indicate that squamous papilloma is a distinct entity not
related to condyloma or verrucous carcinoma. These lesions are benign, HPV DNA
negative, DNA diploid, and they lack p53 overaccumulation. Cancer 2000;88:
1679 – 86. © 2000 American Cancer Society.
KEYWORDS: bladder, neoplasms, squamous lesion, precursor, koilocyte, condylomata acuminata, verrucous carcinoma, papilloma, human papillomavirus, p53, DNA
ploidy.
S
The authors thank Dr. Ricardo V. Lloyd for excellent technical assistance.
Dr. Bostwick’s current address: Bostwick Laboratories, 6722 Patterson Ave., Richmond, VA 23226.
Address for reprints: Liang Cheng, M.D., Department of Pathology, University Hospital 3465, Indiana University School of Medicine, 550 North University Blvd., Indianapolis, IN 46202. Email:
Icheng@iupui.edu.
Received October 8, 1999; revision received December 28, 1999; accepted December 28, 1999.
© 2000 American Cancer Society
quamous papilloma, condylomata acuminatum, and verrucous
carcinoma of the urinary bladder comprise the spectrum of rare
proliferative squamous lesions. There is morphologic overlap between these lesions, and some authors indicate that squamous papilloma and condyloma acuminata of the urinary bladder are histologically indistinguishable,1 although formal evaluation is lacking.
Mostofi et al. stated that some of squmaous papilloma “may be
condyloma acuminata that have extended into the bladder from the
urethra.”2 Some investigators suggest that there is a relation between
squamous papilloma and low grade squamous cell carcinoma, and
that human papillomavirus (HPV) may play an important role in the
development of these squamous proliferations.1–3 However, the correlations among squamous papilloma, condyloma, and verrucous
carcinoma remain largely undefined, and, because of the rarity of the
1680
CANCER April 1, 2000 / Volume 88 / Number 7
TABLE 1
Clinical and Pathologic Findings in 13 Squamous Proliferative Lesions of the Urinary Tract
Case
no.
Age/
gender
Diagnosis
Symptomsa
Cystoscopic
findings
Location
Treatment length of
follow-up (yrs)
1
82 F
Squamous papilloma
Irritative symptomsb
Whitish plaque
Dome
TURB
10.0
2
3
46 F
79 M
Squamous papilloma
Squamous papilloma
Polypoid lesion
Erythematous
Bladder
Lateral wall
None
None
2.0
1.5
4
62 F
Squamous papilloma
Whitish plaque
Vesical neck
TURB
0.3
NED
5
6
7
70 F
32 F
63 F
Squamous papilloma
Squamous papilloma
Squamous papilloma
Not documented
Detected at
surveillance H/O
invasive
urothelial
carcinoma
Irritative symptoms
and Hematuria
Not documented
Not documented
Irritative symptoms
H/O urothelial
carcinoma
Recurrence of
squamous papilloma
at 5 yrs
NED
Died of bladder cancer
—
Papillary lesion
Sessile tumor
Urethra
Urethra
Posterior wall
None
None
TURB
4.3
2.5
8.8
8
45 F
Condyloma acuminatum
Extensive
condyloma
Entire bladder
TURB
15
NED
NED
Nephroureterectomy for
ureter urothelial
carcinoma 7 yrs later
Died of urothelial
carcinoma
Multiple recurrences
Pelvic exenteration
due to perianal
vesical fistula
—
Pelvic exenteration at 4
yrs
Lost to follow-up
9
51 M
Condyloma acuminatum
10
27 M
Condyloma acuminatum
11
81 F
12
13
Irritative symptoms
Extensive vulval
condyloma
Extensive perineal
condyloma
Intravesical
chemotherapy
Lateral wall
vesical neck
Condyloma
Outcome
Condyloma
Entire bladder
—
—
—
Verrucous carcinoma
Extensive urethral
condyloma
Irritative symptoms
Erythematous
Dome
TURB
5.3
62 M
Verrucous carcinoma
H/O bladder calculi
Whitish plaque
Radical cystectomy
5.0
54 F
Verrucous carcinoma
H/O diabetes
Whitish plaque and
erythematous
Trigone, lateral
wall and
dome
Bladder
Recurrence at 1 yr after
diagnosis
Died of cerebrovascular
accident
NED
Unknown
6.0
Reccurence at last
follow-up
H/O: history of; TURB: transurethral resection of the bladder; NED: no evidence of disease.
a
Other than 3 patients with condyloma acuminatum of the bladder (Cases 8, 9, and 10), none of the other patients had history of genital, perineal or perianal condylomas.
b
This patient also had history of interstial cystitis.
lesions, the comparative clinical pathologic features
are not well documented. The objective of this study
was to examine the clinical and histologic features of
squamous papilloma, condyloma acuminatum, and
verrucous carcinoma of the urinary tract. In addition,
HPV DNA in situ hybridization, DNA ploidy determination by image cytometry, and p53 immunostaining
were performed to define the relation between these
squamous proliferative lesions.
MATERIALS AND METHODS
We reviewed cases of squamous papilloma, condyloma acuminata, and verrucous carcinoma of the uri-
nary tract from the Mayo Clinic surgical pathology
files between 1971 and 1998. All patients underwent
transurethral resection. All histologic slides were evaluated by the authors without the knowledge of clinical
information. The 1973 World Health Organization histologic criteria2 were used for the diagnosis of squamous papilloma, which was defined as a papillary
lesion with a delicate fibrovascular stroma lined by
squamous epithelium. The diagnostic criteria for condyloma acuminata and verrucous carcinoma were the
same as those used for other organ sites.3–5 Patient
follow-up was obtained from the medical records.
Routine 5-␮m sections from formalin fixed, par-
Squamous Cell Proliferation of the Bladder/Cheng et al.
1681
FIGURE 1. Squamous papilloma of the
bladder is shown (A and B). The papillary
configuration of the lesion resembles
configurations seen in condyloma.
affin embedded tissue were used for in situ hybridization for HPV detection, immunohistochemical studies,
and DNA ploidy analysis. In situ hybridization was
performed using microwave pretreatment with digoxigenin-labeled probes.6 Briefly, oligonucleotide probes
specific for HPV 6 and 11, HPV 16 and 18, and HPV 31
and 33 (Enzo Diagnostics, Farmingdale, NY) were diluted 1:5 in hybridization solution containing 10%
dextran sulphate, 3⫻ standard saline solution (SCC)
buffer, 1⫻ Denhardt 100 ␮g/mL salmon sperm DNA,
125 ␮g/mL yeast tRNA, 10 ␮g/mL polyadenylic-cytidylic acid, 0.1% sodium pyrophosphate–inorganic,
and 50% deionized formamide. cDNA probes were
applied to pretreated slides, denatured for 5 minutes
at 95 °C, and hybridized for 60 minutes at 37 °C. Slides
were subsequently incubated with an antidigoxigenin
antibody linked to alkaline phosphatase (BoehringerMannheim Biochemicals, Indianapolis, IN) and developed in nitroblue tetrazolium and 5-bromo-chloro-3indolylphosphate. Positive controls consisted of
formalin fixed, paraffin embedded sections of cases
from other organs, such as the cervix, known to be
infected with HPV 6, 11, 16, 18, and 31, 33, 51. Negative
control consisted of substituting another cDNA probe
1682
CANCER April 1, 2000 / Volume 88 / Number 7
TABLE 2
Human Papillomavirus Typing, p53 Alteration, and DNA Ploidy in Squamoproliferative Lesions of the Bladder
HPV type
Case no.
Diagnosis
6/11
16/18
31/33
p53a
DNA ploidy
1
2
3
4
5
6
7
8
9
10
11
12
13
Squamous papilloma
Squamous papilloma
Squamous papilloma
Squamous papilloma
Squamous papilloma
Squamous papilloma
Squamous papilloma
Condyloma
Condyloma
Condyloma
Verrucous carcinoma
Verrucous carcinoma
Verrucous carcinoma
⫺
⫺
⫺
⫺
⫺
⫺
ND
⫹
⫹
⫹
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
ND
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
ND
⫺
⫺
⫺
⫺
⫺
⫺
10
5
5
0
0
0
ND
40
20
20
60
90
95
Diploid
Diploid
Diploid
Diploid
Diploid
Diploid
ND
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
Aneuploid
HPV: human papillomavirus; ND: not done.
a
% of positive staining cells.
(adenovirus) for the HPV probe. All negative slides
were examined for DNA integrity by using an alu
repeat probe (Blur 8, Diagnostic Enzo, Farmingdale,
NY) and were positive for alu repeat DNA sequence.
Immunohistochemical stains were performed on a
Ventana ES autostainer (Tucson, AZ) using the avidinbiotin-complex method. Primary monoclonal antibodies were used for evaluation of p53 (DO-7, Dako,
dilution 1:100). The percentage of immunoreactive
cells was recorded for each case. Positive and negative
controls were run in parallel and gave appropriate
results. Digital image analysis for DNA ploidy was
performed with the CAS 200 digital image analyzer
(Becton Dickinson, Cellular Imaging Systems). Quantification of Feulgen staining was performed with the
quantitative DNA analysis program (version 3.0).
None of these ancillary studies were used in the original file classification and none of the original file
diagnoses were changed after performance of ancillary studies.
RESULTS
Table 1 summarizes the patient characteristics and
clinical findings. None had positive urine culture. Of 7
cases of squamous papilloma (5 in the urinary bladder
and 2 in the urethra), the male-to-female ratio was 1:6
and the mean age was 62 years (range, 32– 82 years).
The mean follow-up was 4.2 years (range, 0.3–10
years). One patient had history of interstitial cystitis
and had recurrence at 5 years after diagnosis (Case 1).
None had history of genital, perineal, or perianal condyloma. Squamous papilloma is characterized by pro-
liferation of squamous epithelium surrounding a central fibrovascular core (Fig. 1). In situ hybridization for
HPV was negative in all cases (Table 2). No or minimal
p53 nuclear accumulation was observed (Table 2). All
squamous papillomas were diploid by digital image
analysis.
Condyloma acuminata of the bladder is indistinguishable from that seen in other organ sites. It shows
papillary growth of squamous epithelium displaying
koilocytosis and nuclear changes characteristic of HPV
infection (Fig. 2). The underlying stroma is well vascularized with scattered lymphocytic infiltration. No
stromal invasion is seen. The adjacent epithelium
showed squamous change with acanthosis and hyperkeratosis. The involvement of bladder by condyloma
acuminata is usually extensive. All three cases of condyloma acuminata of the bladder were associated with
coexistent extensive condyloma acuminata of external
genitalia and were suspected during cystoscopic examinations. All three cases were positive for HPV types
6 and 11 (Fig. 2). Subsequently, two patients underwent pelvic exenteration for uncontrolled condylomas. DNA ploidy analysis revealed aneuploidy pattern
in both cases. Abnormal p53 expression was seen in all
three cases.
Verrucous carcinoma of the bladder is morphologically identical to its counterpart in the oral cavity,
the lower female genital tract, the digestive tract, and
other locations. It is composed of well-differentiated
keratinizing squamous epithelium that invades the
stroma in a pushing fashion. The degree of cytologic
atypia is mild (Fig. 3). None had history of genital,
Squamous Cell Proliferation of the Bladder/Cheng et al.
1683
FIGURE 2. Condyloma acuminata of
the bladder is shown. Koilocytotic
change can be subtle (A), and human
papillomavirus in situ hybridization is
positive in the deeper section (B).
perineal, or perianal condyloma. HPV was not detected by in situ hybridization. Strong p53 nuclear
accumulation and aneuploid tumor population were
observed in all 3 cases (Table 2). The adjacent epithelium was squamous in nature, showing acanthosis
and hyperkeratosis. Two cases (Cases 11 and 13)
showed features that resembled squamous papilloma,
including proliferation of benign-appearing squamous epithelium with underlying dilated vessels; subsequently, both patients developed recurrence of verrucous carcinoma (Table 1). One patient underwent
radical cystectomy and there was no evidence of cancer recurrence during 5 years of follow-up (Case 12).
DISCUSSION
Squamous lesions of the urinary bladder are rarely
encountered, and the distinctions among squamous
papilloma, condyloma acuminata, and verrucous carcinoma are difficult to make in small biopsies.1,3,4,7–9
Because of the morphologic similarity to condyloma,
some investigators have suggested that squamous
papilloma of the bladder is associated with HPV infec-
1684
CANCER April 1, 2000 / Volume 88 / Number 7
FIGURE 3. Verrucous carcinoma of
the bladder is shown. The pushing margins are characteristic of verrucous carcinoma (A). p53 immunostaining is
strongly positive (B).
tion,1–3 although this relation has not been confirmed.
In this study, we found that all squamous papillomas
were negative for HPV DNA, were DNA diploid, and
displayed no or minimal p53 protein nuclear accumulation. These lesions were benign and infrequently
recurred. Our study indicates that squamous papilloma is a distinct entity not related to condyloma or
verrucous carcinoma.
Some investigators have considered that condyloma acuminatum of the bladder morphologically indistinguishable from squamous papilloma1 and postulated that some squamous papillomas may
represent extensions of condylomas from the urethra.2
Clinical information and ancillary studies, such as
HPV DNA in situ hybridization studies, p53 immunostaining, and DNA ploidy analysis, may be useful in
the differential diagnosis (Table 3). Less than 2 dozen
cases of condyloma acuminata3,10 –19 of the bladder
have been reported. The majority of patients had a
history of long-standing uncontrolled condyloma of
the external genitalia, similar to our cases. Isolated
condyloma of the bladder is rare and almost always
presents in immunosuppressed patients.1,11 Del Mistro et al. reported three cases of condyloma, two of
Squamous Cell Proliferation of the Bladder/Cheng et al.
1685
TABLE 3
Differential Diagnosis of Squamous Papilloma, Condyloma Acuminata, and Verrucous Carcinoma of the Urinary Bladder
Age (yrs)
Gender (male:female)
Clinical history
Clinical presentation
Biologic behavior
Location
Extent
Histologic changes
Architecture
Pushing margin
Cytologic atypia
Stromal invasion
p53 alteration
HPV detection
DNA ploidy
a
b
Squamous papilloma
Condyloma acuminataa
Verrucous carcinomab
62 (range, 32–82)
1:6
Nonspecific
Irritative symptoms
Rarely recurs
No predilection
Small, solitary
40 (range, 17–76)
1:1.6
External genitalia condyloma or history of immunosuppression
Irritative symptoms
Aggressive
No predilection
Multiple, extensive
66 (range, 43–83)
1.2:1
Nonspecific
Irritative symptoms
Aggressive
No predilection
Diffuse, extensive
Papillary
Absent
Usually not seen or mild
Absent
⫺/⫹
⫺
Diploid
Papillary
Absent
Usually not seen or mild
Absent
⫹
⫹
Aneuploid
Expansive and endophytic
Present
May be present
Present
⫹⫹
⫺
Aneuploid
References 3, 10–19.
References 22–28.
which occurred in immunocompromised patients and
one in a patient with extensive treatment-resistant
external genitalia condylomata with secondary involvement of the urinary bladder.3 All 3 patients had
multiple recurrences, and their lesions were aneuploid
and positive for HPV DNA types 6 and 11.3 Similarly,
we found that our 3 patients with condylomata had
aneuploid tumors that were HPV DNA positive for
types 6 and 11. All three patients had extensive external genitalia involvement by condylomata, and two
required pelvic exenteration for uncontrolled condylomata. In most reported cases, condyloma of the
bladder is refractory to conservative therapy, necessitating cystectomy in more than half the reported
cases.
The relation between condyloma acuminata and
verrucous carcinoma is not well understood. Most
cases of vesical verrucous carcinoma have occurred in
association with schistosomiasis infection,20 and, to
the best of our knowledge, only eight cases have been
reported without such infection.21–28 Of these eight
unique cases, two had extensive external genitalia
condyloma with secondary involvement of the bladder,21,22 suggesting the possibility of misinterpretation
of the bladder tumor, although HPV typing was not
performed. Alternatively, there may be a relation between verrucous carcinoma and condyloma. We could
not detect HPV DNA in our cases of verrucous carcinoma or any association with schistosomiasis infection. Clearly, additional cases of verrucous carcinoma
are needed to study HPV DNA status. Together with
findings from other studies, squamous papilloma does
not appear to be associated with schistosomiasis or
condyloma, and some verrucous carcinomas apparently are not associated with schistosomiasis or condyloma and have no recognizable connection with
infectious agents or any other predisposing condition.
The diagnosis of verrucous carcinoma relies on the
findings of expansive growth, pushing margins, lack of
well-formed papillae, and cytologic atypia, although
the atypia is mild and usually presents in the deeper
portions of the lesion (Table 3). Condyloma acuminata
is almost always associated with extensive external
genitalia condyloma or immunocompromising conditions, lacks stromal invasion, and is HPV DNA positive
by in situ hybridization.
Several limitations of this study should be considered. The current study includes only a small number
of patients with relatively short follow-up. Nonetheless, this is the first report of squamous papilloma of
the bladder with follow-up, HPV analysis, DNA ploidy
determination, and p53 immunostaining. We were not
able to demonstrate HPV infection in squamous papilloma, although the possibility of some unusual types
of HPV as etiologic agents cannot be ruled out. The
sensitivity of our HPV analysis may also be limiting,
because approximately 50 or more copies of HPV DNA
are necessary for in situ hybrization detection. If an
infected sample has less than 50 copies of HPV DNA,
this could lead to false-negative results.6 More sensitive methods, such as in situ polymerase chain reaction (PCR), in situ reverse PCR, and self-sustained
sequence replication, may yield a higher detection
rate.29 The possible link between squamous papilloma
and condyloma could not be established by the current investigation. Furthermore, the value of ancillary
1686
CANCER April 1, 2000 / Volume 88 / Number 7
studies may be limited in small cystoscopic biopsies
because intralesional heterogeneity of DNA content
and expression of HPV and p53 potentially influences
interpretation. In addition, the cystoscopic examinations may be nonspecific, and the findings of whitish,
plaquelike lesions should alert the urologists and pathologists to consider these unusual squamous lesions.
Squamous papilloma is a benign lesion that is
HPV DNA negative and DNA diploid and lacks p53
overaccumulation. In contrast, condyloma acuminatum is clinically aggressive, frequently recurrent, usually associated with extensive external genitalia involvement, HPV DNA positive, and DNA aneuploid,
and exhibits abnormal p53 protein accumulation. Verrucous carcinoma is an indolent neoplasm that is HPV
negative and DNA aneuploid and exhibits abnormal
p53 accumulation. Although the limitations discussed
above are relevant, our results indicate that squamous
papilloma is a distinct entity not related to condyloma
or verrucous carcinoma. The assessment of DNA
ploidy status, p53 alteration, and HPV DNA by in situ
hybridization may be of value in distinguishing among
these unusual squamous lesions in select cases.
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