Benign Mimics and Tumor-like Lesions in Urologic Pathology
Moderators: Dr. Mahul Amin and Dr. Liliane Boccon-Gibod
Section 3 -
Tumor-like Lesions of the Urinary Bladder
Robert H. Young
In this lecture I will present important areas in differential diagnosis of benign versus
malignant in the urinary bladder, covering some time-honored lesions, but ones about which there is, in
some instances, new information and a spectrum of other entities whose features have largely only been
appreciated in recent years.
von Brunn's Nests
This term refers to the presence of groups of transitional cells in the lamina propria,
detached from the overlying urothelium. These are common findings, which are frequently associated with
the closely related abnormalities cystitis glandularis and cystitis cystica. The nests arise by a
process of invagination from the overlying urothelium and the term von Brunn's is used when an attachment
to the urothelium is still present. It is the detachment from the overlying epithelium seen in von
Brunn's nests that can be problematic, particularly if the nests lie relatively deep in the lamina
propria, and are numerous. The cystoscopic impression may be of a "tumor" , which may enhance
diagnostic problems. Even when deeply located or numerous these are often rounded, invariably well
circumscribed, nests of transitional cells. The Hopkins group has contributed a very good recent study
on this process, emphasizing its potential for misdiagnosis as cancer . Although the nests of this
process are generally rounded and smoothly contoured as I have just noted, they pointed out that they
maybe somewhat irregular. They emphasized the important fact that there depth of "penetration" into the
lamina propria is usually to a uniform depth, giving a somewhat band-like sense to the admittedly
somewhat problematic, in some cases, busy proliferation. It is helpful that invasive carcinoma of the
bladder usually exhibits irregular infiltration of the stroma by nests of cells and single cells with
moderate to marked atypia, has an associated stromal response and does not have the band-like aspect just
noted. Even when invasive carcinoma has relatively bland cytologic features, the cell nests generally
have a more disorderly arrangement and more variation in size and shape than von Brunn's nests. Although
the bland cytology of the cells in von Brunn's nests in most cases contrasts with the significant atypia
seen in most invasive bladder cancers, the epithelium in von Brunn's nests, like the surface epithelium,
may exhibit hyperplasia and reactive atypia including prominent nucleoli and mitotic activity. Some of
the most striking cases of von Brunn's nests are actually seen in the renal pelvis or ureter in my
This process occurs when gland lumens develop in von Brunn's nests. In its commonest
(non-intestinal) form cystitis glandularis is characterized by glands lined by cuboidal to columnar cells
which are themselves usually surrounded by a layer of transitional cells. This change may also involve
the surface mucosa. This process rarely causes concern for malignancy and indeed the converse error,
under diagnosing carcinoma with luminal differentiation for cystitis glandularis of typical type is
probably more common, although still rare. Deviations from an orderly architecture of the type
considered in the presentation of von Brunn's nests are again helpful.
In contrast to the typical form of cystitis glandularis, the cells lining the glands in
some cases of cystitis glandularis, referred to as the intestinal type , are tall and columnar with
abundant mucin. These cells may be admixed with goblet cells and the epithelium often closely resembles
intestinal epithelium; Paneth cells and argentaffin or argyrophil cells are also rarely present. The
surface urothelium may also undergo similar intestinal-type mucinous metaplasia. The two types of
cystitis glandularis may coexist, although one of them is often the exclusive or predominant type in a
Although usually a microscopic finding, cystitis glandularis of usual type is occasionally
visible grossly as an irregularity of unimpressive nature. More worrisome appearing, fleshy polypoid
lesions may be present in cases of the intestinal type of cystitis glandularis, and occasionally the
radiologic or cystoscopic appearance suggests a malignant tumor. On microscopic examination the lesion
usually occurs in a non-polypoid mucosa but occasionally an exuberant proliferation produces a papillary
or polypoid lesion helping to explain the occasional case, which simulates a neoplasm at cystoscopy.
Cystitis glandularis of the intestinal type, although more problematic than the usual
type, should uncommonly cause serious diagnostic problems for the pathologist because the atypicality in
most adenocarcinoma exceeds that seen in cystitis glandularis and irregular, stromal infiltration
generally makes the diagnosis of adenocarcinoma easy. However, cases are encountered in which
distinction from adenocarcinoma is difficult. Cases in which there is an irregular disposition of the
glands in the stroma, glands deep in the lamina propria and cytologic atypia, even if minor, should be
evaluated cautiously as all these features increase the likelihood of the glands being neoplastic. It
should be emphasized that mucin extravasation may be striking in cases of the intestinal variant of
cystitis glandularis . In contrast to colloid carcinoma clusters of epithelial cells are not seen
floating in the mucin and the lining epithelium of cysts is not malignant appearing.
The great majority of cases of cystitis glandularis that have been associated with
malignancy have been of the intestinal type and the major significance of the intestinal-type of cystitis
glandularis rests in this association. Mucinuria is a clinical clue to the presence of mucinous
metaplasia in some cases and if persistent or prominent, should raise the suspicion of carcinoma,
particularly if the clinical setting, such as the presence of a neurogenic bladder, is known to
predispose to mucinous metaplasia and subsequent neoplasia. In patients with a non-functioning bladder
mucinous metaplasia may be particularly extensive. In some cases there has been a very long history of
prolonged cystitis glandularis of intestinal type before an adenocarcinoma has evolved. In cases of
adenocarcinoma arising on a background of intestinal metaplasia varying degrees of precancerous
atypicality up to adenocarcinoma in situ may be seen.
Friedman and Kuhlenbeck  named this lesion "nephrogenic adenoma" because in its
commonest form it is composed of small tubules that resemble renal tubules. This process has generally
been thought to be metaplastic, and the terms "nephrogenic metaplasia" or "adenomatous metaplasia" are
preferred by some. A recent paper  suggested that the lesion may actually be of renal tubular origin,
an issue that I will not get into here as it does not bear on the practical benign versus malignant
issue. Approximately 80 percent of the cases involve the bladder, but the urethra has been involved in
12 percent and the ureter in 8 percent . Urethral cases are actually the most difficult to evaluate
because the clear cell carcinoma that may be somewhat difficult to distinguish from nephrogenic adenoma
is commoner in the urethra than the bladder.
Although most common in adults, approximately 10 percent of the reported cases have been
encountered in children. The great majority of nephrogenic adenomas are associated with a history of an
operative procedure on the genitourinary tract (61 percent of the cases), or one or more irritants
including calculi (14 percent of the cases), trauma of various types (9 percent of the cases) and
cystitis. Additionally, approximately 8 percent of the patients have been the recipients of a renal
transplant. About 60 percent of the patients have had symptoms such as hematuria, frequency, or dysuria
but because of the frequent presence of other lesions it is usually unclear whether a given symptom can
be attributed to the nephrogenic adenoma.
At cystoscopy nephrogenic adenoma may simulate a papillary, sessile or in-situ carcinoma.
Approximately fifty-six percent of the lesions are papillary, 10 percent polypoid, and 34 percent
sessile. The lesions vary from incidentally discovered microscopic lesions to masses up to 7 cm in
greatest dimension. Approximately 62 percent are 1 cm or less, 28 percent between 1 and 4 cm and 10
percent over 4 cm. They are typically single but approximately 18 percent are multiple; rarely there is
diffuse involvement of the bladder.
On microscopic examination tubular, cystic, polypoid, papillary, and rarely diffuse
patterns are encountered. The tubules are usually small, round and hollow but are occasionally larger,
elongated and solid. They are sometimes surrounded by a prominent basement membrane, which is
highlighted if a periodic-acid-Schiff stain is performed. Having heard several authorities speak on
nephrogenic adenoma, it is clear that the frequency of this change is variable according to different
experiences. I personally have not found it as frequent as some clearly have. If present, it can be a
helpful diagnostic finding, but I simply think it is present in a distinct minority of cases. The
tubules frequently undergo varying degrees of cystic dilatation and cysts, which are present in most
cases, sometimes predominate. The tubules and cysts may contain an eosinophilic or basophilic secretion,
which usually stains weakly positive with the mucicarmine stain. Papillae are less common than tubules
and cysts but are not rare. Occasionally larger, broader, polypoid structures are present. Foci with a
diffuse, almost solid growth may be seen in nephrogenic adenomas but are uncommon and always limited in
extent. These are actually due to fusion of tiny tubules with imperceptible lumens imparting a solid
appearance except on very close high-power scrutiny.
The majority of the cells lining the tubules, cysts and papillae are cuboidal to low
columnar with scant cytoplasm, but cells with abundant clear cytoplasm are occasionally present lining
these structures and in the solid areas. Hobnail cells line the tubules and cysts in about one third of
the cases and large cysts may be lined by flattened cells. Small amounts of mucin may be present in the
cells of nephrogenic adenoma but glycogen is absent or scanty in our experience. Nuclear atypia is
uncommon, and when present appears degenerative in nature; nucleoli may be prominent . Mitoses are
absent or very rare. There is often marked chronic cystitis which may partially obscure the nephrogenic
adenoma and rare cases have been associated with prominent stromal calcification.
Several features of nephrogenic adenoma may cause particular diagnostic difficulty and
merit emphasis. Tiny tubules containing mucin and apparently lined by a single cell with a compressed
nucleus may simulate signet ring cells. The haphazard distribution of the tubules may also simulate the
appearance of an invasive adenocarcinoma, a resemblance that is enhanced when the tubules are admixed
with the muscle fibers that may be found in the lamina propria. Hobnail cells may suggest the diagnosis
of the rare clear cell carcinoma of the bladder, particularly because the latter, like nephrogenic
adenoma, has tubular, cystic and papillary patterns. A solid growth of cells with clear cytoplasm may
also raise the possibility of clear cell carcinoma. Clear cell carcinoma is less common in the bladder
than in the urethra  and in our experience distinction between nephrogenic adenoma and clear cell
carcinoma is more troublesome in the urethra particularly within urethral diverticula . In men
nephrogenic adenoma of the prostatic urethra may be somewhat challenging
particularly as it is
often seen after a transurethral resection in a patient with prostatic cancer and recurrence of the
latter is sometimes suggested. The morphology of prostatic carcinoma and nephrogenic adenoma are usually
distinctly different, however, although I have rarely seen tubular glands of prostate carcinoma quite
reminiscent of the tubules of nephrogenic adenoma. If needed immunohistochemistry can help in this
regard . Although it is well known that nephrogenic adenoma and prostatic adenocarcinoma can,
treacherously, both be positive for P504S, in contrast to nephrogenic adenoma, prostatic adenocarcinoma
is positive for PSA and negative for epithelial membrane antigen . Although they persist and/or
recur in about one-third of the cases, nephrogenic adenomas are benign. Evidence presented suggesting
that nephrogenic adenoma is a precursor of clear cell carcinoma of the bladder is not convincing in our
opinion. The fact that clear cell carcinoma is much more common in the urethra and in women whereas
nephrogenic adenoma is more common in the bladder and in men also argues against such a relationship.
At cystoscopy, or on microscopic examination, this lesion may be confused with
transitional cell carcinoma . The designation papillary cystitis is used when thin finger-like
papillae are present, and polypoid cystitis when the lesions are edematous and broad based. In both
papillary and polypoid cystitis there is typically prominent chronic inflammation in the stroma and blood
vessels, some of them ectatic, may be conspicuous. A spectrum of appearances ranging from papillary
cystitis to polypoid cystitis to bullous cystitis is encountered, depending on the amount of stromal
edema. In bullous cystitis the lesion is wider than it is tall, whereas in both polypoid and papillary
cystitis the reverse is true. It is the predominantly exophytic character of polypoid and papillary
cystitis that may cause confusion with carcinoma. As papillary and polypoid cystitis are associated with
inflammation they may be associated with metaplastic changes in the urothelium covering them, or adjacent
to them. There are two particular clinical settings, which should suggest that an exophytic bladder
lesion may be inflammatory. These are cases in which there is an indwelling catheter and cases of
vesical fistula, the latter being particularly treacherous if the clinical history is not provided to the
The most important differential diagnosis of papillary and polypoid cystitis is with
papillary transitional cell carcinoma. Cases of papillary and polypoid cystitis without a history of
catheterization are particularly likely to be considered carcinomas at cystoscopy. On gross inspection
and microscopic examination, however, the fronds of polypoid cystitis are typically much broader than
those of a papillary carcinoma. The thin papillae of papillary cystitis are more difficult to
distinguish from carcinoma. In the former (as in polypoid cystitis) the urothelium may be hyperplastic,
but usually is not as stratified as in a carcinoma; additionally, umbrella cells are more often present.
The fibrovascular cores of the papillae of a transitional cell carcinoma typically lack the prominent
inflammation that characterizes both papillary and polypoid cystitis, and the edema seen in the latter.
Large papillae of a transitional cell carcinoma also often give rise to smaller papillae, a feature not
associated with papillary or polypoid cystitis.
The well-known changes of radiation injury seen elsewhere in the body such as atypia of
epithelial cells and so-called radiation fibroblasts in the stroma may be seen in the bladder but a
particularly treacherous facet of radiation injury in the bladder, the formation of so-called
pseudocarcinomatous proliferations, has recently been emphasized
In these cases irregularly
shaped and arranged aggregates of epithelial cells in the upper and middle zones of the lamina propria
can produce a very confusing picture architecturally. Small pseudopods may heighten the resemblance to
carcinoma and retraction artifact around them may suggest they are sitting in vessels. When the cells
show radiation atypia the potential for confusion with carcinoma is even higher. In such cases the
picture, although obviously suspicious, is not typical of early invasive transitional cell carcinoma and
that observation should always prompt a search for other findings consistent with radiation injury, which
are typically present. These include radiation fibroblasts, prominent vascular ectasia, abundant fibrin
deposition, stromal fibrosis and squamous metaplasia.
Features of the epithelial proliferation in these cases in addition to the associated
findings just noted, that may be helpful, include focal squamous differentiation (although it must be
acknowledged that that may be seen in transitional cell carcinoma), and peculiar wrapping of the
proliferating epithelial cells around vessels, a feature highlighted in particular in one recent
contribution . That article also drew attention to the fact that rarely a similar process may be
seen in patients undergoing chemotherapy.
The bladder is involved in approximately one percent of women with endometriosis and is
the commonest site of urinary tract involvement by this disease. Up to fifty percent of the patients
have a history of a pelvic operation and in approximately 12 percent of them evidence of extra-vesical
endometriosis is lacking. Vesical endometriosis is commonest in the fourth decade with the average age
of 35 years. The microscopic features of endometriosis are so distinctive that confusion with a neoplasm
should not be an issue. This is in marked contrast to the other mullerian glandular lesions which are
Glandular lesions characterized by a prominent component of endocervical-type epithelium
may involve the wall of the urinary bladder in women of reproductive age and have been designated
"endocervicosis" . A mass that ranges up to 2.5 cm. is typically located in the posterior wall or
posterior dome. Microscopic examination typically reveals extensive involvement of the involved bladder
wall by irregularly disposed benign appearing or milding atypical endocervical-type glands some of which
are cystically dilated. Occasionally one may find ciliated cells or a minor component of endometrioid
glands and glands lined by non-specific cuboidal or flattened cells with eosinophilic cytoplasm. In some
cases the glands are associated with fibrosis or edema in the adjacent stroma. Rarely there is some
evidence of endometriotic stroma indicating a relationship of this lesion to endometriosis. This, and
other features, such as an occasional association with a history of a cesarean section indicate that this
is a unique mullerian lesion of the bladder and it is best considered the mucinous analogue of
endometriosis. It is important because lack of awareness of it may lead to confusion with an
adenocarcinoma, particularly one of urachal origin. Adenocarcinomas of the bladder, particularly or
urachal origin, may have glands lined by tall mucin-rich epithelial cells and as these cancers and
endocervicosis both occur at the dome one might think their distinction might be challenging. However,
as will be discussed in more detail in my second lecture, urachal adenocarcinomas broadly speaking fall
in two groups, overtly infiltrating lesions with obvious malignant characteristics ruling out
endocervicosis, or lower grade mucinous cystic lesions with differing gross characteristics. In some
cases of benign mullerian lesions foci of endosalpingiosis are also present and when endometriosis and
endocervicosis are present as well the designation "mullerianosis" has been suggested .
Spindle Cell Lesions
Atypical, mononucleated or multinucleated mesenchymal cells are a relatively frequent
finding in the lamina propria of the bladder . In my experience cells of this type are relatively
common in routine biopsies without obvious evidence of cystitis. The cells often have tapering
eosinophilic cytoplasmic processes and may simulate both smooth or skeletal muscle cells. Their nuclei
are typically hyperchromatic and often irregular in size and shape but mitotic figures are typically
absent. The cells resemble those that may be seen in the stroma of the female genital tract. Similar
cells may be seen in patients treated with chemotherapeutic agents and radiation. These atypical stromal
cells occasionally confuse the inexperienced but rarely cause serious diagnostic problems. In one
unusual case large numbers of them in the stroma of a fibroepithelial polyp caused diagnostic difficulty
Much more problematic are florid myofibroblastic proliferations that may form grossly
evident masses and that have been such a source of recent interest in the literature, one of the largest
studies having just appeared . Terminology is an issue here.
In the paper just cited , those
reactive to a recent procedure and those that were not were grouped together. I disagree with this
approach because it downplays the importance of the clinical background in pathology, which is a
discipline founded on the importance of clinicopathologic correlation. Perhaps I am old fashioned but I
also believe when an entity is characterized by two of the legendary figures in anatomic pathology, they
are owed continuation of "their entity" unless there is pressing evidence that it is doing harm. With
that preamble, I will now discuss the two variants, as I see it, of this entity, the first, because of
its crisp clear association with a recent procedure being considered first.
(i) Postoperative Spindle Cell Nodule
From the mid 1970s through the early 1980s Drs. Rosai and Scully saw cases of florid
spindle cell proliferations in the genitourinary tract that were usually considered malignant by others
but which they thought were benign because of the clinical background. The unifying clinical feature of
the cases was the development of the lesions three months or less after a surgical procedure had been
performed at the site from which the lesional tissue was obtained. Two of the lesions in men were in
specimens obtained by transurethral resection (T.U.R.) of the bladder. They each had had a T.U.R. of the
bladder performed two months previously. At cystoscopy "heaped up tumor" and a "friable vegetant mass"
were noted. The designation postoperative spindle cell nodule was given to the entity when the first
report was made in 1984 .
Microscopic examination shows intersecting fascicles of spindle cells, which often show
conspicuous mitotic activity. A marked resemblance to a sarcoma, particularly leiomyosarcoma, often
results. Additional microscopic features which are often present include a delicate network of small
blood vessels scattered acute and chronic inflammatory cells, small foci of hemorrhage, mild to moderate
edema and focal myxoid change in the stroma. Despite the generally numerous mitotic figures, the cells
do not exhibit marked cytologic atypia. The clinical association with a recent operation was the major
initial clue that these lesions represented an exuberant reactive proliferation. This interpretation was
supported by the benign outcome, with conservative management, of the initially reported cases and those
The interpretation of spindle cell lesions of the urinary bladder and in particular the
confident diagnosis of a postoperative spindle cell nodule is amongst the most difficult in urologic
pathology. Although other sarcomas, such as Kaposi's sarcoma, occasionally are suggested, leiomyosarcoma
is usually the major consideration in differential diagnosis. Distinction from a moderate to poorly
differentiated leiomyosarcoma is not difficult as the atypia in these cases exceeds that seen in a
postoperative spindle cell nodule (PSCN). However, many well-differentiated leiomyosarcomas do not
appear more atypical cytologically than a PSCN and may be less mitotically active than a PSCN. Although
one might expect destructive growth to be helpful in this differential, the PSCN may invade the muscular
wall of the bladder. Although leiomyosarcomas may be vascular, the often prominent delicate network of
small blood vessels that is seen in many PSCN is, in our opinion, more in keeping with a diagnosis of
PSCN than sarcoma. Myxoid change may be seen in both the PSCN and leiomyosarcoma and is not particularly
helpful diagnostically, although prominent myxoid change is more in favor of a leiomyosarcoma.
The PSCN may stain positively for cytokeratin . Ultrastructural studies of the PSCN
are limited but the cells in the few cases studied have been more characteristic of myofibroblasts than
smooth muscle cells. Therefore, features of unequivocal smooth muscle differentiation favor a diagnosis
of sarcoma in this context, although we would not wish to rely only on this feature to differentiate the
two lesions. Ultimately, distinction between these two processes is very dependent on the clinical
history of a recent operative procedure. In occasional cases in our experience it has been impossible to
make a confident distinction between them particularly when the interval between a prior operative
procedure and the development of a spindle cell lesion is longer (over 3 months) than in most cases of
PSCN. In these cases careful clinical follow-up with repeat cystoscopy and further biopsies is
indicated. Conservative excision of a grossly visible lesion is also justified.
(ii) Inflammatory Pseudotumor
The first issue to be addressed here is terminology. A variety of terms have been used
for this process over the years
Terms such as that used in a recent excellent study
"Pseudosarcomatous Myofibroblastic Proliferations" , seem to have begun to dominate in recent times,
but I am not a great enthusiast for that terminology for the following reason. It is at least somewhat
similar to the "inflammatory myofibroblastic tumor" used for a separate entity considered neoplastic and
typically occurring in children, but with at least some morphologic overlap. I just find this confusing
even reading the literature. One of the best early studies of this entity  used the term
inflammatory pseudotumor and to me it is the best available because more likely than not this does have
an inflammatory background and it certainly is a pseudotumor in the tradition of using that word for a
mass-like lesion that is non-neoplastic.
This lesion may occur at any age but typically occurs in adults in the middle years of
life. On gross examination the majority have had an exophytic character often forming striking polypoid
intraluminal masses but occasionally a sessile, endophytic appearance is observed. On microscopic
examination the characteristic microscopic appearance is that of spindle cells typically relatively
widely separated in a vascular myxoid sometimes basophilic stroma. Less commonly a more compact cellular
less myxoid appearance reminiscent of a plasma cell granuloma variant of inflammatory pseudotumor is
observed and indeed it is probable that the occasional plasma cell granuloma of the bladder reported is
in this category of lesion. Ultrastructural examination has typically shown the features of
myofibroblasts. On microscopic examination the differential diagnosis of this lesion is similar to that
of the postoperative spindle cell nodule both myxoid sarcomas and myxoid areas in sarcomatoid carcinoma
 occasionally being major considerations.
Immunostaining for ALK1 may be of diagnostic aid
It should be mentioned that occasional inflammatory pseudotumors, like the post-operative spindle cell
nodule, may be immunoreactive for keratin ,
indeed strikingly so in one recent series . The
diagnosis of a reactive mesenchymal lesion in the bladder should be made with great caution in these
cases in which there is no history of a recent operation, which is so helpful in cases of postoperative
spindle cell nodule. That having been said, there is no doubt that a sarcoma-like proliferation that is
benign occurs in the bladder and irrespective of the preferred designation it is crucial that this be
distinguished from malignant processes for obvious therapeutic and prognostic reasons.
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