Urinary bladder melanosis associated with urothelial dysplasia and invasive urothelial Carcinoma

ArticleinAnalytical and quantitative cytology and histology / the International Academy of Cytology [and] American Society of Cytology 35(5):294-300 · October 2013with115 Reads
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Abstract

Melanosis is defined as an abnormal or excessive deposition of melanin within cells and/or tissues. It typically presents as a cutaneous or buccal mucosal lesion, but rare cases of bladder melanosis have also been documented. Melanosis of the urinary bladder is typically considered a benign condition, but it has also been described in association with malignant melanoma and urothelial carcinoma. We report the cases of 2 patients who presented with melanosis of the urinary bladder. One patient presented with melanosis of the urinary bladder together with urothelial dysplasia. Melanosis was incidentally identified during a cystoscopy for ureteral stones. A second patient presented with hematuria and was found to have a muscle invasive urothelial carcinoma with focal small nested morphology together with melanosis. We also present a literature review of the bladder melanosis and an overview of other bladder melanocytic lesions, which include primary and metastatic melanoma and blue nevus. Initial evaluation for bladder melanosis should include cystoscopy and upper urinary tract imaging. Biopsy is essential to establish the diagnosis and rule out associated malignancy.

Full-text

Available from: Kiril Trpkov, Nov 18, 2014
1
BACKGROUND: Melanosis is defined as an abnormal
or excessive deposition of melanin within cells and/or
tissues. It typically presents as a cutaneous or buccal
mucosal lesion, but rare cases of bladder melanosis have
also been documented. Melanosis of the urinary bladder
is typically considered a benign condition, but it has also
been described in association with malignant melanoma
and urothelial carcinoma.
CASES: We report the cases of 2 patients who presented
with melanosis of the urinary bladder. One patient pre-
sented with melanosis of the urinary bladder together
with urothelial dysplasia. Melanosis was incidentally
identified during a cystoscopy for ureteral stones. A sec-
ond patient presented with hematuria and was found to
have a muscle invasive urothelial carcinoma with focal
small nested morphology together with melanosis. We
also present a literature review of the bladder melanosis
and an overview of other bladder melanocytic lesions,
which include primary and metastatic melanoma and
blue nevus.
CONCLUSION: Initial evaluation for bladder melanosis
should include cystoscopy and upper urinary tract imag-
ing. Biopsy is essential to establish the diagnosis and rule
out associated malignancy. (Anal Quant Cytopathol
Histopathol 2013;35:000–000)
Keywords: bladder; blue nevus; carcinoma, transi-
tional cell; melanoma; melanosis; urinary bladder;
urothelial carcinoma.
Melanosis is characterized by an abnormal or ex-
cessive deposition of melanin pigment within cells
and/or tissues. It typically presents as cutaneous
or buccal mucosal lesion. Melanosis of the urinary
bladder (or melanosis vesicae) is extremely rare,
with only 16 cases reported in the English litera-
ture.
1-14
Of those 16 patients 11 had only simple
melanosis,
1-8
2 had urothelial cell carcinoma and
melanosis,
9,10
and 3 patients had melanoma and
melanosis.
12-14
Athough melanosis has been con-
Analytical and Quantitative Cytopathology and Histopathology
®
0884-6812/13/3500-0000/$18.00/0 © Science Printers and Publishers, Inc.
Analytical and Quantitative Cytopathology and Histopathology
®
Urinary Bladder Melanosis Associated with
Urothelial Dysplasia and Invasive Urothelial
Carcinoma
A Report of 2 Cases
Premal Patel, B.H.Sc., Alex Kavanagh, M.D., Samir Al Bashir, M.D.,
Tarek A. Bismar, M.D., Geoffrey Gotto, M.D., M.P.H., and Kiril Trpkov, M.D., FRCPC
From the Department of Medicine, University of Calgary; the Department of Medicine, University of British Columbia; and the De-
partment of Pathology and Laboratory Medicine and the Division of Urology, University of Calgary and Calgary Laboratory Services,
Canada.
Mr./Ms.? Patel is ____________, Department of Medicine, University of Calgary.
Dr. Kavanagh is ______________, Department of Medicine, University of British Columbia.
Dr. Al Bashir is _____________, Department of Pathology and Laboratory Medicine, University of Calgary and Calgary Laboratory Ser-
vices.
Dr. Bismar is ____________, Department of Pathology and Laboratory Medicine, University of Calgary and Calgary Laboratory Services.
Dr. Gotto is ____________, Division of Urology, University of Calgary.
Dr. Trpkov is ____________, Department of Pathology and Laboratory Medicine, University of Calgary and Calgary Laboratory Services.
Address correspondence to: Kiril Trpkov, M.D., FRCPC, Rockyview General Hospital, 7007 14 Street, Calgary, Alberta T2V 1P9, Canada
(kiril.trpkov@cls.ab.ca).
Financial Disclosure: The authors have no connection to any companies or products mentioned in this article.
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sidered a benign condition, its association with
malignancy in recent reports raises questions about
its pathogenesis and relationship with associated
malignancy.
In this report we describe 2 additional patients
with melanosis. The first patient had melanosis
which was discovered incidentally during cys-
toscopy for ureteral stones. Bladder biopsy also
showed urothelial dysplasia, but carcinoma in situ
(CIS) and invasive carcinoma were not present. The
second patient presented with hematuria and was
found to have a muscle invasive urothelial carci-
noma together with melanosis. We also review the
previously published melanosis cases, with and
without associated malignancy, and we discuss the
other melanocytic lesions of the urinary bladder.
Case Reports
Case 1
A 60-year-old male with no smoking history pre-
sented to the emergency room with intractable left
flank pain but without lower urinary tract symp-
toms. He was not taking any prior medications and
had no significant comorbidities. No fever or other
significant symptoms were documented at presen-
tation. Physical examination revealed left costo-
vertebral angle tenderness but was otherwise un-
remarkable, and in particular, no other cutaneous
or mucosal lesions were identified. Urinalysis re-
vealed large leukocytes, negative nitrites and a
moderate amount of blood in the urine. A noncon-
trast computerized tomography scan of the ab-
domen and pelvis revealed an obstructing calculus
in the proximal left ureter associated with hydro-
nephrosis. The initial cystoscopic appearance of the
bladder mucosa is shown in Figure 1. During cys-
toscopic evaluation of the bladder, diffuse brown-
black mucosal pigmentation was observed, which
persisted after irrigating the bladder lumen several
times to clear the dark sediment. Ureteric orifices
were not involved. Several areas of raised pigment-
ed urothelium were also noted. The lesions were
deemed clinically suspicious for malignancy, and
a biopsy was performed. The patient was treated
with a 6-week course of Ciprofloxacin, and a repeat
cystoscopy after 3 months revealed clearing of the
mucosal pigmentation and showed essentially
normal mucosa. No biopsy was performed at that
time. Another 6-week course of Ciprofloxacin was
continued and a cystoscopy was planned after 3
months; the patient, however, did not attend the
follow-up appointment. After 12 months from the
initial presentation the patient did not present again
to clinical attention. Of note, pigmentation of the
bladder mucosa was not identified 7 years prior to
the presentation with melanosis, when the patient
had renal colic caused by ureteric calculus.
Pathology Findings. The bladder biopsy demon-
strated diffuse dark brown–black pigment with
powdery to coarse granular features within the
superficial lamina propria, which only focally and
minimally involved the overlying urothelium (Fig-
ure 2A). Urothelium showed focal dysplasia with
cytologic and architectural abnormalities, but frank
CIS and invasive urothelial carcinoma were not
present (Figure 2B). The pigment stained black by
Masson Fontana (Figure 2C) and disappeared after
bleaching (Figure 2D). The pigment was negative
for iron (Prussian blue), and was consistent with
melanin. S100 and HMB-45 immunohistochemical
stains were negative, showing absence of mucosal
melanocytes, but CD68 highlighted scattered histi-
ocytes in superficial lamina propria containing
melanin. p53 and Cytokeratin 20 highlighted the
areas of urothelial dysplasia.
Case 2
A 69-year-old female presented with gross hema-
turia, rapidly increasing creatinine and bilateral hy-
2
Analytical and Quantitative Cytopathology and Histopathology
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Patel et al
Figure 1 Cystoscopic appearance of brown/black pigmentation
of the bladder mucosa (case 1).
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dronephrosis. Previously she was generally healthy
with no documented comorbidities and she was not
taking any medications. No history of allergies was
documented. On cystoscopic evaluation an infiltra-
tion of black-colored tumor was seen, involving the
trigone and extending toward the right lateral wall.
Both ureteric orifices were obscured by the tumor,
which was visibly necrotic. Transurethral resection
of the bladder tumor and insertion of J-stents were
performed. A follow-up bone scan was negative,
and multiple nonenlarged lymph nodes were pres-
ent in the mediastinum. She subsequently present-
ed to emergency with recurrent rising creatinine
(120–370 ng/mL). A Foley catheter was inserted
and replacement of her ureteric stents and IV hy-
dration were performed, which did not improve
her renal function. The patient was not considered
a candidate for radical surgery, although systemic
chemotherapy was discussed; however, 2 months
later she passed away.
Pathology Findings. Biopsy showed high-grade uro-
thelial carcinoma invasive into muscularis propria
(Figure 3B and C). Invasive carcinoma showed areas
of small nested morphology, suggestive of small
nested variant of urothelial carcinoma. Extensive
coagulative tumor necrosis was present. Black,
crystalline to globular pigmented material was
present in the superficial lamina propria (Figures
3A and D). This pigment was mostly deposited
within histiocytes in the lamina propria, which
were reactive for CD68. Masson-Fontana showed
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Urinary Bladder Melanosis
Figure 2 (A) Extensive melanosis in superficial lamina propria with minimal involvement of normal urothelium. (B) Area of urothelial
dysplasia with focal melanosis in superficial lamina propria. (C) Masson Fontana shows diffuse black pigmentation in lamina propria,
consistent with melanin. (D) No pigment is present after bleaching (same field).
A
B
CD
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black staining which disappeared after bleaching.
Additional special stains for iron, calcium, bile and
copper staining were negative.
Discussion
Melanocytic lesions of the bladder are extremely
rare. They include benign entities, such as bladder
melanosis and blue nevus, and malignant ones
such as primary and secondary melanoma. All of
these should be considered in the differential diag-
nosis of a melanocytic lesion of the bladder. Bladder
melanosis has been considered a benign condition;
however, recent case reports, including this one,
document its association with preneoplastic or
neoplastic lesions. Primary or secondary malignant
melanoma of bladder is also exceptionally rare, and
the clinical correlation is essential to rule out a met-
astatic lesion. Lastly, blue nevus of the bladder has
been reported only once in the English literature,
with reports in other organs documenting its be-
nign nature. Herewith, we provide a literature re-
view of the melanocytic lesions of the bladder.
Bladder Melanosis
Melanosis of the urinary bladder is an exceptional-
ly rare entity, with only 16 cases reported in the
English literature (Table I).
1-14
Patient age in report-
ed cases ranged from 43–86 years, with no gender
predilection. Symptoms at the time of presentation
included hematuria,
5,8,9,11,12,14
urinary obstruction,
9
recurrent cystitis,
1,10
incontinence,
2,4,7
painless ab-
dominal mass,
13
dysuria,
3
overactive bladder,
6
and
in 1 of the patients in this report, renal colic. On cys-
toscopic evaluation melanosis presents as brown to
4
Analytical and Quantitative Cytopathology and Histopathology
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Patel et al
Figure 3 Diffuse melanosis in (A) mucosal lamina propria and in (B) high-grade invasive urothelial carcinoma. (C) Carcinoma showed
focal small nested pattern. (D) Masson Fontana shows diffuse black pigmentation in lamina propria, consistent with melanin.
A
B
C
D
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black mucosal pigmentation with flat or punctuate
patterns, and all areas of the bladder can be affect-
ed. No mass lesions were documented in previous
reports; however, the first patient in this report
presented with several raised areas of urothelium,
corresponding with the foci of urothelial dysplasia,
which was previously not reported in association
with melanosis. The first patient in this study also
had a transient melanosis (it disappeared after 3
months). Because melanocytes are not typically
present within the urinary bladder, it has been spec-
ulated that melanosis may occur as a result of aber-
rant migration of these cells from the neural crest
during embryological development. Other theories
postulated that melanocytes within the urinary
bladder may derive from aberrant differentiation of
urothelial stem cells.
1,15
However, S100 and HMB-
45 immunohistochemical stains were negative in
both cases in this report, indicating absence of
mucosal melanocytes. Bladder melanosis was pre-
viously associated with adriamycin toxicity
16
in 1
patient, but no other association has been docu-
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Urinary Bladder Melanosis
Table I Reported Cases of Bladder Melanosis Including the Cases from this Report
Author/year Age/sex Symptoms Medications Follow-up/management
Melanosis
Alroy et al, 1986
11
71/F Bloody urethral discharge Methyldopa
Triamterene
Hydrochlorothiazide
72/M Urinary obstruction
Chong et al, 1999
2
86/F Urinary incontinence
Dysuria
Rossen et al, 1999
1
44/F Recurrent cystitis
43M Gross hematuria
Wieringa et al, 2006
8
52/M Gross hematuria
Di Fiore et al, 2007
3
72/M Dysuria Frequent antibiotics
Malodorous urine
Jin et al, 2009
4
77/F Urinary incontinence Tolterodine
Urgency with leakage
Sen Gupta et al, 2010
5
84/M Gross hematuria
Talmon et al, 2010
6
56/F Overactive bladder 6 mos, NOD
Willys et al, 2011
7
73/F Chronic incontinence Phenytoin
Intermittent voiding dysfunction Thyroxine
Isosorbide mononitrate
Telmisartan
Atorvastatin
Ezetimibe
Acetylsalicylic Acid
Nitrolingual spray
Current study 60/M Intractable left flank pain 12 mos
Melanosis associated with urothelial cell carcinoma
Sanborn et al, 2008
9
63/F Multiple urinary tract infections 12 mos (management
unknown)
Harikrishnan et al, 2012
10
50/M Loin pain and gross hematuria Nephroureterectomy
Current study 69/F Gross hematuria, acute renal failure 3 mos, DOD
Melanosis associated with melanoma
Ainsworth et al, 1976
14
65/F Gross hematuria; firm, movable mass, Cystectomy
5–7 cm, palpable through anterior
vaginal wall
Kerley et al, 1991
12
80/F Vulvar melanosis, malignant melanoma 18 mos, DOD; cystectomy,
of clitoris. 2 years later developed THBSO
gross hematuria
Kojima et al, 1992
13
63/F Painless mass, 5 mm, right posterior;
enlarging over 6 mos
NOD = no evidence of disease, DOD = dead of disease, THBSO = total hysterectomy and bilateral salpingo-oophorectomy.
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mented in previously reported cases. Melanosis
was also identified adjacent to primary malignant
melanoma of the bladder.
12-14
Some authors have
proposed that melanosis may represent a melano-
ma precursor lesion because of the presence of atyp-
ical melanocytes.
6
However, no study so far docu-
mented a progression of the melanosis to malignant
melanoma to support this theory.
The biopsy is paramount in establishing the cor-
rect diagnosis because the differential diagnosis of
mucosal pigmentation includes also primary or
metastatic melanoma and hemosiderin or lipo-
chrome pigment deposition.
10
A blue nevus has
been only recently documented in the bladder and
can also be considered in the differential diagnosis.
Although melanosis is usually considered a benign
condition, given the paucity of documented cases
in the literature and with only a short follow-up of
1 year or less, it is difficult to completely rule out the
possibility that melanosis represents a premalig-
nant lesion in all cases.
Melanosis was also identified in association with
urothelial carcinoma in 2 previously reported pa-
tients in addition to the 1 patient in this report. One
of the previously reported patients was a 63-year-
old woman presenting with gross hematuria and
recurrent urinary tract infections. On cystoscopy
she was found to have melanosis of the bladder.
After 1 year she developed a high-grade urothelial
carcinoma invading into the lamina propria of the
bladder (pT1) and CIS. At that time no melanosis
was documented. The patient was treated with
transurethral resection and intravesical Bacillus
Calmette-Guérin therapy. Follow-up cystoscopy at
3 months revealed no recurrence of urothelial car-
cinoma, and melanosis was not apparent at that
time.
9
In another previously reported patient, dif-
fuse bladder melanosis was found in a setting of
a synchronous high-grade urothelial carcinoma,
which was invading the distal ureter (pT2). This pa-
tient was a 50-year-old male who presented with
flank pain and gross hematuria and subsequently
underwent nephroureterectomy
10
; however, no
follow-up was provided. We document a third pa-
tient who presented with invasive urothelial carci-
noma with focal small nested pattern together with
melanosis. The association of melanosis with small
nested variant of urothelial carcinoma has also not
been previously reported. Therefore, bladder mela-
nosis may also present with high-grade urothelial
carcinoma either in synchronous or metachronous
fashion.
Bladder Melanoma
Primary malignant melanoma of the genitourinary
tract is a rare entity and accounts for only 0.2% of all
melanomas.
17
According to a recent review a pri-
mary bladder melanoma has been reported in only
19 patients.
18
Primary bladder melanoma occurs
with equal frequency in men and women, with an
age range of 44–81 years. Gross hematuria is the
most frequent presentation.
12
Macroscopically it
can appear as a dark brown to black, polypoid or
fungating lesion and or it may be solid or infiltrat-
ing,
14
although the pigmentation may be mild or
even absent.
18
Microscopically the lesions appear
ulcerated with islands or solid sheets of atypical,
variably pigmented melanocytes with differing
invasion within the bladder wall. Tumor cells may
appear large, epithelioid or spindle-shaped with
variably pigmented cytoplasm, oval nuclei, and
prominent nucleoli. Marked pleomorphism may
also be noted along with giant cells and atypical
mitotic figures. The cells stain for S100, HMB-45
and Melan-A.
19
It is crucial to differentiate primary
bladder melanoma from metastatic bladder mel-
anoma by following the criteria set by Ainsworth
and coworkers
9
:
No history of melanoma of the skin or other
site
Examination of the entire skin surface, includ-
ing the use of a Woods light to exclude depig-
mented areas that may represent regressed
melanoma
Clinical studies to exclude an ophthalmic or
other visceral primary site
The pattern of metastases or recurrence should
be consistent with a primary bladder tumor
rather than metastatic melanoma
No widespread metastasis 16 months after the
primary diagnosis
Atypical melanocytes present adjacent to the
tumor nodule.
Two-thirds of the patients with bladder melanoma
have died of metastatic melanoma within 3 years of
the diagnosis.
19
Bladder Blue Nevus
Only 1 case has been reported previously of bladder
blue nevus. A 72-year-old woman with a past his-
tory of breast cancer presented with lower abdom-
inal pain and hematuria. Transurethral resection
was undertaken which showed urothelial mucosa
with intact surface urothelium overlying an intra-
vesical tumor. The tumor cells showed strong
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positivity for HMB-45, Melan-A, and weak positive
staining for S100 protein. The cells were negative
for various keratin markers, but CD117/c-kit was
strongly positive. No mutations were found in
BRAF, NRAS, or CKIT. A postoperative PET scan
showed no evidence of disease. A follow-up cys-
toscopy and bladder biopsy 8 months later showed
a small residual tumor with morphological and im-
munohistochemical features similar to the previous
specimen. After a short follow-up of only 9 months,
no recurrence or metastasis were identified.
20
Blue
nevus is characterized by spindled melanocytes
with dendritic processes; however, it may also in-
clude a variety of other cell types. This leads to di-
agnostic dilemma as both melanoma and cellular
blue nevus are often characterized by dense cellu-
larity, lack of “maturation,” deep extension, abun-
dant pigmentation, and range of epithelioid to
spindle-shaped cells. Melanoma can be differentiat-
ed from blue nevus based on the expansile growth
with possible necrosis and heterogeneous pigmen-
tation. An invasion of lymphoid cells may also be
present. In contrast, blue nevus typically has a uni-
form appearance at low power microscopy. Pig-
mentation is prominent in macrophages at the
periphery. Immunohistochemical stains for HMB-
45, S100, and Melan-A cannot distigush between
the two because both lesions stain positive. Prolifer-
ation marker Ki-67 tends to be higher in melanomas
(often > 10%) than in cellular blue nevus (usually
< 5%).
20
Conclusion
Melanosis of the urinary bladder is a rare and usu-
ally benign condition, but infrequently it can be
associated with urothelial malignancy or preneo-
plastic lesions. Initial evaluation should include
cystoscopy and upper urinary tract imaging. Biop-
sy is essential in establishing the diagnosis and in
ruling out associated malignant or preneoplasic
lesions, as well as other melanocytic lesions of the
bladder, such as primary or secondary melanoma
or blue nevus. Although follow-up is not warranted
in the majority of cases, it may be necessary in
patients presenting with subsequent hematuria or
other symptoms.
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