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853
Atypical Nephrogenic Metaplasia of the Urinary Tract
A Precursor Lesion?
Liang Cheng, M.D.1
John C. Cheville, M.D.2
Thomas J. Sebo, M.D., Ph.D.2
John N. Eble, M.D.1
David G. Bostwick, M.D.2
1
Department of Pathology, Indiana University
School of Medicine, Indianapolis, Indiana.
2
Department of Pathology, Mayo Clinic, Rochester, Minnesota.
BACKGROUND. Nephrogenic metaplasia with cytologic atypia (atypical nephrogenic
metaplasia) is occasionally encountered and its biologic potential is uncertain.
METHODS. The authors describe 18 cases of atypical nephrogenic metaplasia characterized by the presence of prominent cytologic atypia, including nuclear enlargement, nuclear hyperchromasia, and enlarged nucleoli. DNA ploidy analysis by
digital image analysis and immunostaining for high-molecular-weight cytokeratin
(34␤E12), cytokeratin 7, cytokeratin 20, carcinoembryonic antigen (CEA), epithelial
membrane antigen (EMA), p53, and MIB-1 were performed in 9 cases.
RESULTS. The mean patient age was 62 years (median, 65 years; range, 39 – 84
years). The male-to-female ratio was 2.6:1. Two patients had a history of noninvasive papillary urothelial carcinoma. The typical clinical presentation was hematuria (8 patients) and voiding symptoms (5 patients). Cystoscopic findings were
suspicious for neoplasm in 7 of 13 cases. The neoplastic cells were positive for
high-molecular-weight cytokeratin, cytokeratin 7, and EMA, and were usually
negative for cytokeratin 20 and CEA. p53 nuclear accumulation and increased
MIB-1 labeling index were seen in 4 cases. DNA ploidy analysis showed aneuploid
pattern in 2 of 9 cases. The mean patient follow-up was 3.5 years (range, 0.5–10.6
years); 2 patients had recurrent nephrogenic metaplasia, and the remainder were
alive without recurrence or urothelial carcinoma.
CONCLUSIONS. Atypical nephrogenic metaplasia is benign; it occasionally displays
substantial cytologic abnormalities of no apparent clinical significance. Awareness
of the spectrum of cytologic changes within this entity is critical to prevent
overdiagnosis of cancer and avoid unnecessary treatment. There is no direct
evidence that links atypical nephrogenic metaplasia to cancer. Cancer 2000;88:
853– 61. © 2000 American Cancer Society.
KEYWORDS: bladder, nephrogenic metaplasia, urinary tract, atypia, precursor,
urothelial carcinoma, adenocarcinoma.
N
Current address for Dr. Bostwick: Bostwick Laboratories, 6722 Patterson Ave., Richmond, VA
23226.
Address for reprints: Liang Cheng, M.D., Department of Pathology, UH 3465, Indiana University
School of Medicine, 550 North University Blvd.,
Indianapolis, IN 46202. Email: lcheng@iupui.edu
Received June 9, 1999; revision received September 7, 1999; accepted September 30, 1999.
© 2000 American Cancer Society
ephrogenic metaplasia of the bladder is a common mimic of
adenocarcinoma which presents a diagnostic challenge in the
interpretation of bladder biopsies.1–7 Cases with cytologic atypia,
which we refer to as atypical nephrogenic metaplasia (ANM), are
occasionally encountered, but have not been previously described
with follow-up data. We report the clinical, pathologic, DNA ploidy,
proliferation index, and immunohistochemical characteristics of 18
cases of ANM.
MATERIALS AND METHODS
We reviewed all cases of nephrogenic metaplasia of the urinary tract
in the Mayo Clinic surgical pathology files from the years 1981–1998.
Eighteen cases of atypical nephrogenic metaplasia (ANM) were retrieved, including nine from the consultation files of one of the
854
CANCER February 15, 2000 / Volume 88 / Number 4
TABLE 1
Atypical Nephrogenic Metaplasia of the Urinary Tract
Case
no.
Age
(yrs)/
gender
1
2
84/M
72/M
3
4
Endoscopic
findings
Location
Size
(mm)
Multifocality
Treatment
Follow-up
(yrs)
Outcome
Erythematous
Erythematous
Vesical neck
Bladder diverticulum
5
1
No
No
None
None
1.0
0.5
ANED
ANED
53/F
20/M
Obstructive symptoms
Hematuria and
recurrent urinary
tract infection
Hematuria
Reflex uropathy
Erythematous
Neoplasm
Posterior wall
Base and posterior
wall and trigone
5
3
No
Yes
None
None
3.3
10.6
5
62/M
Hematuria
Neoplasm
3
Yes
None
2.0
6
63/F
Hematuriaa
Erythematous
Lateral and posterior
wall, and dome
Right and left lateral
wall
Dead of other causes
Recurrent nephrogenic metaplasia
2 yrs later, subsequent biopsies
negative. No evidence of
disease at the last follow-up
ANED
4
Yes
None
4.4
7
63/F
Papillary
lesion
Lateral wall
4
No
None
5.9
8
70/M
Neoplasm
Base
2
No
None
3.2
Dead of other causes
9
10
11
12
13
48/M
39/M
70/F
72/M
68/M
Irritative symptom
and H/O interstitial
cystitis
Hematuriaa H/O
noninvasive
urothelial
carcinoma
Hematuria
H/O hydronephrosis
Hematuria
Obstruction
—
Recurrent nephrogenic metaplasia
half a yr later. No evidence of
disease at the last follow-up
ANED
Erythematous
—
Neoplasm
Neoplasm
—
1
7
6
5
1
No
No
No
No
No
None
—
—
None
—
3.0
—
—
1.0
—
ANED
—
—
Dead of other causes
—
14
15
48/M
79/M
6
1
No
No
—
—
—
—
—
—
16
63/M
17
74/M
Residual nephrogenic metaplasia
at cystectomy
—
18
75/F
—
Clinical presentation
Hematuria
Urinary calculi and
recurrent urinary
tract infection
—
—
Erythematous
Lateral wall
Bladder
Lateral wall
Bladder
Diverticulum of
urethra
Prostatic urethra
Posterior wall
—
Lateral wall
—
No
H/O noninvasive
urothelial
carcinoma
—
Papillary
tumor
Prostatic urethra
2
No
Radical
cystectomyb
—
—
Bladder
1
No
—
ANED: alive with no evidence of disease; H/O: history of; TCC: transitional cell (urothelial) carcinoma; -: unknown.
a
History of radiation therapy for cervical carcinoma one year prior to the diagnosis.
b
This case was initially diagnosed as adenocarcinoma at another institution, and the patient was subsequently treated by radical cystectomy 3 mos after the diagnosis.
authors (D.G.B.). ANM was defined as the presence of
cytologic atypia, including nuclear enlargement, nuclear hyperchromasia, and prominent nucleoli. Patient follow-up was obtained in all cases from the
medical records and direct contact with referring clinicians and pathologists.
All immunohistochemical stains were performed
on a Ventana ES autostainer (Tucson, AZ) using the
routine avidin-biotin-complex method. Antibodies
applied for immunostaining included high-molecularweight, basal cell specific anticytokeratin (34␤E12,
1:10 dilution, monoclonal (Dako, Carpinteria, CA), an-
ticytokeratin 7 (1:100 dilution, monoclonal), anticytokeratin 20 (1:100 dilution, monoclonal, Dako), anti–
carcinoembryonic antigen (1:25 dilution, monoclonal,
Dako), anti– epithelial membrane antigen (1:20 dilution, monoclonal, Dako), anti-p53 (D0-7, 1:100 dilution, monoclonal, Dako), and anti-MIB-1 (1:20 dilution, monoclonal, Dako). Positive and negative
controls were run in parallel and gave appropriate
results.
The specimens were examined for deoxyribonucleic acid (DNA) ploidy by digital image analysis,8 and
DNA histograms were classified as diploid, tetraploid,
FIGURE 1. Atypical nephrogenic metaplasia (Case 12) is shown. (A) Papillae and tubules are common patterns. (B) Multiple nucleoli are present in some cells.
(C) Large nucleoli are present. (D) Inflammatory cells are invariably present, and a few multinucleated epithelial cells are also present. (E) Immunostaining for
high-molecular-weight cytokeratin (34␤E12) is shown. (F) Immunostaining for cytokeratin 7 is shown.
FIGURE 1. (continued)
Atypical Nephrogenic Metaplasia/Cheng et al.
857
FIGURE 2. Atypical nephrogenic metaplasia is
shown. (A) Prominent nucleoli and intraluminal
mucin secretion are readily seen (Case 13). (B)
Case 15 shows intraluminal mucin secretion and
clear cell changes, mimicking signet ring cell
adenocarcinoma.
or aneuploid. Quantification of MIB-1 (Ki-67) labeling
was performed using the CAS 200 digital image analyzer and proliferation index software programs (Beckton Dickinson, Cellular Image System, San Jose, CA).9
RESULTS
The clinical findings in 18 cases of ANM are summarized in Table 1. The mean patient age was 62
years (median, 65 years; range, 39 – 84 years); the
male-to-female ratio was 2.6:1. Two had histories of
noninvasive papillary urothelial carcinoma. The
typical clinical presentation was hematuria (8 patients) and voiding symptoms (5 patients). Cystoscopic findings were suspicious for neoplasm in 7 of
13 cases. There was no apparent predilection of
bladder location.
ANM was usually unifocal, small (mean, 4 mm in
greatest dimension; range, 1– 6 mm), and well circumscribed. Various growth patterns, including tubular,
papillary, and solid growth, were seen. Most of the
cells lining tubules, cysts, and papillae were cuboidal
or low columnar with scant cytoplasm (Fig. 1). Prominent nucleoli were readily visible (Figs. 1–2). Luminal
mucin production (71%) (Fig. 2), hobnail cells (53%),
and clear cell change (35%) were common (Table 2).
Mitotic figures were absent, and there was no necrosis. ANM usually occurred in a background of acute
and chronic inflammation and stromal edema, and
often coexisted with squamous metaplasia (22%) or
cystitis glandularis (24%). Stromal calcifications were
present in two cases. One case (Case 16) was misinterpreted as adenocarcinoma at another institution,
858
CANCER February 15, 2000 / Volume 88 / Number 4
TABLE 2
Atypical Nephrogenic Metaplasia of the Urinary Tract:
Histopathologic Findings
Findings
No. of cases (%)
Superficial location
Lobular growth
Stromal edema
Chronic inflammation
Luminal mucin
Acute inflammation
Hobnail cells
Solid pattern
Clear cell change
Cystitis glandularis
Squamous metaplasia
Multifocality
Stromal calcification
Mitotic figures
Necrosis
18/18 (100)
18/18 (100)
16/18 (89)
15/18 (83)
12/17 (71)
10/18 (56)
9/17 (53)
8/17 (44)
6/17 (35)
7/17 (24)
4/18 (22)
3/18 (17)
2/17 (12)
0/17 (0)
0/17 (0)
and the patient subsequently underwent cystectomy;
no cancer was found in the final specimen.
Table 3 summarizes the results of DNA ploidy
analysis, MIB-1 labeling index, p53 protein nuclear
accumulation, and other immunohistochemical
stains. An aneuploid DNA pattern was detected in
two of nine cases (case 2 and 12). All cases displayed
positive immunoreactivity for high-molecular-weight
cytokeratin (34␤E12), cytokeratin 7, and EMA. Focal
positivity for cytokeratin 20 was detected in 1 case.
Positive immunostaining for CEA was evident in 3
cases. p53 nuclear accumulation (range, 0 –20%) and
increased MIB-1 labeling index (range, 0 –5%) occurred in 4 cases (Table 3).
The mean follow-up was 3.5 years (range, 0.5–10.6
years). Two patients had recurrent nephrogenic metaplasia (none had cytologic atypia), and none had
carcinoma in situ or urothelial carcinoma at last
follow-up.
DISCUSSION
Atypical nephrogenic metaplasia is characterized by a
circumscribed proliferation of tubules, cysts, and papillae lined or covered by cells with enlarged hyperchromatic nuclei and prominent nucleoli. In this
study, we examined the clinical, pathologic, DNA
ploidy, proliferation index, and immunohistochemical
features of 18 cases of ANM. We found that patients
with ANM usually presented with hematuria and/or
voiding symptoms. Cystoscopic findings were often
suspicious for neoplasm. Aneuploid DNA pattern, p53
nuclear accumulation, and increased MIB-1 labeling
index occurred in some lesions. However, ANM was
benign, and none of the patients developed urothelial
carcinoma, adenocarcinoma, or carcinoma in situ
during a mean follow-up period of 3.5 years.
Nephrogenic metaplasia is a metaplastic process
of the urinary tract, including the bladder (55%), urethra (41%), and ureter (4%).4 It probably represents a
host response to local traumatic irritation, such as a
surgical or cystoscopic procedure, chronic infection,
calculi, prolonged catheterization, intravesical therapy, or renal transplantation. Typically, nephrogenic
metaplasia occurs in adults (mean age, 52 years) with
male predilection (male-to-female ratio ⫽ 2:1).4 Clinical presentations include hematuria, frequency, and
dysuria. It may be cystoscopically indistinguishable
from a small papillary urothelial neoplasm; therefore,
biopsies are recommended.10,11 Nephrogenic metaplasia is usually small (⬍1 cm) and solitary.1 Microscopically, tubules are the most common histologic
finding, but the proliferation may also be cystic, polypoid, papillary, and, on rare occasions, diffuse and
solid. The tubules are circumscribed and surrounded
by prominent basement membranes, and often contain eosinophilic or basophilic secretions that are
weakly mucicarminophilic.
Cytologically abnormal cells may occur in nephrogenic metaplasia.2– 4,12–17 ANM is characterized by
the presence of enlarged hyperchromatic nuclei and
prominent nucleoli. This cytologic atypia raises the
diagnostic consideration of adenocarcinoma. In men,
the presence of enlarged nucleoli is suggestive of prostatic adenocarcinoma, especially if the lesion occurs in
the bladder neck or the prostatic urethra. Nine of our
18 cases of ANM were referred to one of authors
(D.G.B.) because of the unusual cytologic appearance,
underscoring the diagnostic concern. Published reports on ANM are limited. Malpica et al.12 found that
“the nucleoli were occasionally prominent” in their
eight cases of nephrogenic metaplasia of the prostatic
urethra. Mild to moderate nuclear atypia was seen in
8 of 15 reported cases.2 Oliva and Young found prominent nucleoli at least focally in 20% of their 80 reported cases,4 and mild to moderate nuclear atypia
was frequent.2 Due to the paucity of reports of these
unusual findings, it is not surprising that misinterpretation of ANM has occurred.18 One case was initially
reported by a pathologist as signet ring cell adenocarcinoma.18
There is no convincing evidence linking nephrogenic metaplasia to cancer. A recent cytogenetic study
indicated that some examples of nephrogic metaplasia
harbor the same genetic alterations as urothelial carcinoma.19 The authors of that study postulated that
these lesions may exhibit an aggressive phenotype.19
Nephrogenic metaplasia may show monosomy 9 and
trisomy 7 and may coexist with vesical urothelial car-
Atypical Nephrogenic Metaplasia/Cheng et al.
859
TABLE 3
Immunohistochemical Findings and DNA Ploidy Analysis of Atypical Nephrogenic Metaplasia
Case no.
34␤E12
CK7
CK20
CEA
EMA
p53 (%)
MIB-1 (%)
DNA ploidy
1
2
3
5
6
7
8
9
12
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
Focal positivity
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫺
⫹
⫺
⫺
⫺
Focal positivity
⫺
⫺
⫺
Focal positivity
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
⫹
5
0
10
10
20
10
0
0
20
1.4
0
0
0
1.5
0.4
0
0
5
Diploidy
Aneuploid
Diploid
Diploid
Diploid
Diploid
Diploid
Diploid
Aneuploid
34␤E12: high-molecular-weight cytokeratin; CK: cytokeratin; CEA: carcinoembryonic antigen; EMA: epithelial membrane antigen; ⫹: positive; ⫺: negative.
TABLE 4
Differential Diagnosis of Atypical Nephrogenic Metaplasia and Clear Cell Adenocarcinoma
Characteristics
ANM
Clear cell adenocarcinoma
Gender
Male predominance
(male-to-female ratio, 2.6:1)
62
Hematuria and voiding symptoms
Benign
No apparent predilection
Small (mean, 3.9 mm)
Female predominance
(male-to-female ratio, 1:18)
58
Hematuria and voiding symptoms
Aggressive
(21% died within 4 yrs)
Urethrab
Large
Absent
Absent or inconspicuous
Common
Common
May be seen
Common
Usually absent
Absent
Invariably present
Often present (53%)
Easily identifiable
Uncommon
Common
Common
Common
Present
May be seen
May present
Present
Present
Present
Minimal
Present
Present
Present
Present
Negative
Positive
Positive
Negative
Positive
⬍5%
Occasional positive
Aneuploid pattern may be seen
Negative
Positive (occasionally negative)
Unknown
Unknown
Positive
Often ⬎15%
Positive
Unknown
Mean age (yrs)
Clinical presentation
Biologic behavior
Location
Size
Microscopic findings
Necrosis
Mitotic figures
Stromal edema
Luminal mucin
Clear cell change
Hobnail cells
Infiltrative growth
Psammoma bodies
Inflammation
Cytologic atypia
Nuclear enlargement
Nuclear hyperchromasia
Prominent nucleoli
Nuclear pleomorphisma
Immunostaining
PSA
34␤E12
Cytokeratin 7
Cytokeratin 20
EMA
MIB labeling index
p53
DNA ploidy
PSA: prostate specific antigen; 34␤E12: high-molecular-weight cytokeratin; EMA: epithelial membrane antigen.
a
Nuclear pleomorphism is more pronounced in clear cell adenocarcinoma.
b
Clear cell adenocarcinoma of the urinary bladder is rare, and the diagnosis should be made with extreme caution.
860
CANCER February 15, 2000 / Volume 88 / Number 4
cinoma;11,20,21 however, malignant transformation has
not been reported. Tse et al.20 studied 22 patients with
nephrogenic metaplasia and observed that 6 had coexisting bladder carcinoma, including 1 with nephrogenic metaplasia arising within urothelial carcinoma.
With less than 2 years of follow-up, none underwent
malignant transformation.20 In another study of vesical nephrogenic metaplasia in renal transplant recipients, all cases were diploid and recurrent lesions
remained diploid.22 The authors concluded that nephrogenic metaplasia lacked malignant potential.22 Similarly, a diploid DNA pattern was found by Gaylis et
al.23 In our study, none of the patients, including 2
patients with aneuploid ANM, developed malignancy
during a mean follow-up period of 3.5 years. It appears
that ANM is not biologically different from typical
nephrogenic metaplasia and may be merely an unusual type of metaplastic transformation of urothelial
cells without malignant potential. The importance of
recognizing this lesion is to avoid misinterpretation or
overdiagnosis of cancer. However, the findings of DNA
aneuploid in two cases and the limited length of our
follow-up warrant caution in the interpretation of our
data.
The most important differential diagnostic consideration with ANM is clear cell adenocarcinoma (Table 4).1–5,24 –26 The greatest difficulty in separating
ANM from cancer is encountered in the interpretation
of small, poorly oriented biopsies. Oliver and Young
reviewed a large series of clear cell adenocarcinoma
arising in the urethra, and found that clear cell adenocarcinoma occurred predominantly in elderly
women (male-to-female ratio ⫽ 1:17).24 Mitotic figures were easily found in all cases, and necrosis was
present in 53%.24 Alsanjari et al. found that the presence of solid islands, increased number of mitotic
figures (⬎1 of 10 high-power fields), and increased
MIB-1 labeling index (⬎14%) were helpful in distinguishing clear cell adenocarcinoma from nephrogenic
metaplasia.26 Gilcrease et al. believed that the findings
of severe cytologic atypia, a predominance of clear cell
change, high MIB-1 labeling index, and strong p53
(⬎15%) immunoreactivity were suggestive of clear cell
carcinoma rather than nephrogenic metaplasia.7 ANM
is often composed of mucin-containing tubules lined
by single hobnail cells with clear cytoplasm and prominent nucleoli, closely mimicking clear cell adenocarcinoma. In some cases, it may be composed of diffuse
solid growth of clear cells with cytologic atypia. The
features that we consider helpful to distinguish ANM
from cancer are circumscribed growth, confinement
within the lamina propria, small size of the lesion,
absence of necrosis, absence of mitotic figures, absence of nuclear pleomorphism, the presence of adja-
cent acute and chronic inflammation, and stromal
edema. Unlike clear cell adenocarcinoma, ANM had
no predilection for women or for urethral location.
Cystitis glandularis and squamous metaplasia may coexist with ANM. The findings of clear cells, mucin
production, diffuse solid growth, hobnail cells, and
p53 immunostaining are not specific and may be seen
in both ANM and clear cell adenocarcinoma. ANM is
distinguished from prostatic adenocarcinoma by positive high-molecular-weight cytokeratin (34␤E12)
staining and negative prostate specific antigen staining. DNA ploidy and p53 immunostaining were not
helpful in distinguishing ANM from cancer.
In summary, we describe here a series of cases of
ANM with clinical follow-up. Our observations indicate that ANM is a benign lesion without apparent
malignant potential. Although ANM is unlikely a precursor of bladder carcinoma, it should be considered
in the differential diagnosis of adenocarcinoma, and
awareness of this entity may avoid misinterpretation
or overdiagnosis of cancer.
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