Original Articles
Primary Low-Grade B-Cell Lymphoma of
Mucosa-Associated Lymphoid Tissue Type Arising
in the Urinary Bladder
Report of 4 Cases With Molecular Genetic Analysis
Jaudah Al-Maghrabi, MD, FRCPC; Suzanne Kamel-Reid, PhD; Michael Jewett, MD, FRCS; Mary Gospodarowicz, MD, FRCPC;
Woodrow Wells, MD, FRCPC; Diponkar Banerjee, MBChB, FRCPC, PhD
● Context.—Primary lymphoma of the urinary bladder is
rare. Only 84 cases have been reported in the English literature to date, and none of these cases has had molecular
confirmation of clonal immunoglobulin gene rearrangement.
Objectives.—To review all cases with primary urinary
bladder lymphoma in our records, to classify them using
the REAL classification, to confirm their immunophenotype and genotype, and to determine their outcome.
Design.—We identified 4 cases of primary urinary bladder lymphoma in our medical records from a 30-year period. Immunohistochemical detection of immunoglobulin
light chains and molecular analysis of immunoglobulin
heavy-chain genes using the polymerase chain reaction
were performed on paraffin-embedded material.
Results.—All patients were older than 60 years. The
male-female ratio was 1:3. All patients had a history of
chronic cystitis. Histologic features of mucosa-associated
lymphoid tissue lymphoma with centrocyte-like cells, plasmacytoid B cells, or both were observed in all cases. Monoclonality of B cells was demonstrated by immunohistochemistry, polymerase chain reaction, or both methods in
every case. All patients presented with stage IAE disease,
were treated with radiotherapy alone, and have been in
continuous complete remission for 2 to 13 years.
Conclusions.—Primary bladder lymphomas are usually
of low-grade mucosa-associated lymphoid tissue type. They
are more common in females and are associated with a
history of chronic cystitis. Lymphoepithelial lesions are
seen only in association with areas of cystitis glandularis.
B-cell clonality is readily demonstrable by immunohistochemistry and/or polymerase chain reaction analysis. Local
radiotherapy appears to confer long-term control.
(Arch Pathol Lab Med. 2001;125:332–336)
P
We report 4 additional cases of MALT lymphomas of
the urinary bladder seen at the Princess Margaret Hospital, Toronto, Ontario, during the last 30 years.
rimary malignant lymphoma of bladder is a rare disease, accounting for only 0.2% of all cases of extranodal lymphoma in North America.1 The prognosis of primary bladder lymphoma has been favorable, with many
patients alive and well several years after treatment. A
large proportion of primary lymphomas of the bladder are
lymphomas of mucosa-associated lymphoid tissue
(MALT).2 Mucosa-associated lymphoid tissue lymphomas
were first described by Isaacson and Wright3 in the gastrointestinal tract. Both low- and high-grade B-cell lymphomas arising in MALT have been recognized, the majority of these being low grade. Recently, this concept has
been extended as cases have been described in other sites,
including lung,4–6 trachea,7 thymus,8 skin,9 meninges,10 gall
bladder,11 salivary gland,12 thyroid,13,14 conjunctiva,15,16
breast,17 sinonasal cavities,18 and urinary bladder.2,19–24
Accepted for publication September 15, 2000.
From the Departments of Laboratory Medicine and Pathobiology (Drs
Al-Maghrabi, Kamel-Reid, and Banerjee), Surgical Oncology (Dr Jewett), and Radiation Oncology (Drs Gospodarowicz and Wells), Princess
Margaret Hospital, University Health Network, University of Toronto,
Toronto, Ontario.
Reprints: D. Banerjee, PhD, MBChB, FRCPC, Department of Pathology, Vancouver Cancer Centre, British Columbia Cancer Agency, 600
W 10th Ave, Vancouver, British Columbia, Canada V5Z 4E6.
332 Arch Pathol Lab Med—Vol 125, March 2001
MATERIALS AND METHODS
We searched medical records at the Princess Margaret Hospital
for cases of primary bladder lymphoma. Four cases were found
from a period of 30 years (1969–1999). The clinical histories were
reviewed and are summarized in Table 1. Blocks were recut and
sections stained with hematoxylin-eosin. Immunohistochemical
studies were performed on paraffin sections using the avidinbiotin peroxidase complex, and the panel of antibodies included
those against CD45, CD45RO, CD20, CD43, k and l light chains
(Dako Corporation, Carpinteria, Calif), CD5, CD10 (Novocastra
Laboratories, Ltd, Newcastle Upon Tyne, United Kingdom). Bcell monoclonality was assessed using polymerase chain reaction
(PCR), which was performed on DNA extracted from paraffinembedded tissue, using methods described previously.25 For PCR
analysis, 500 ng to 1 mg DNA was amplified using the appropriate primer, electophoresed through a 2% agarose gel, and visualized using ethidium bromide. Appropriate positive controls,
negative controls, and internal controls were run with each specimen. Polymerase chain reaction analysis was done using primers
specific for the framework 3 (FR3A) and J consensus regions of
the immunoglobulin heavy-chain gene (JH), essentially as described by Trainor et al.26 A second PCR using consensus primers
specific for framework 256 regions and J consensus regions27 was
Low-Grade B-Cell Lymphoma of MALT Type—Al-Maghrabi et al
Table 1. Clinical Summary of Cases
Case No.
1
2
3
4
Age, y/Sex
Presentation
64/F
69/F
72/F
62/M
Hematuria and frequency
Frequency and urgency
Hematuria and nocturia
Hematuria and urgency
also used to increase our detection rate. Internal control primers
were multiplexed with each reaction to ensure the presence of
amplifiable DNA, as described previously.28
REPORT OF CASES
Case 1
A 64-year-old woman presented in 1985 with episodic hematuria and urinary frequency, and was diagnosed to have recurrent urinary tract infection. Multiple urine cultures revealed
staphylococci, streptococci, Escherichia coli, and diphtheroid bacillus species. She had been treated with repeated courses of antibiotics during a 3-year period. Cystoscopy revealed extensive
patches of uneven mucosa involving most of her bladder, as well
as a small area of ulceration. A diagnosis of lymphocytic lymphoma was reported on the basis of a cold cup biopsy. The tumor
involved part of the left ureter. Intravenous pyelography revealed
bilateral hydroureters. Chest radiography, abdominal computed
tomography, and lymphangiogram were normal. Bone marrow
biopsy and aspirate revealed no involvement, and the tumor was
staged as IAE disease. She received radiation therapy to the bladder and pelvis (35 Gy in 20 fractions) and was followed with
cystoscopy every 6 months. She was last seen in May 1999 and
had no evidence of recurrence.
Case 2
In 1993, a 69-year-old woman presented to her family physician with urinary frequency and urgency, and was diagnosed to
have urinary tract infection. Multiple urine cultures showed E
coli infection. No lymphadenopathy was detected. Chest, cardiac,
and abdominal examinations were unremarkable. She was placed
on antibiotics. The patient’s symptoms did not improve, and at
cystoscopy 2 mucosal nodules were observed. Computed tomographic scan of the abdomen showed right hydronephrosis with
a dilated right ureter and some thickening of the bladder wall
consistent with a bladder tumor. Retrograde pyelogram could not
be performed because of obstruction of the distal ureter. A bladder biopsy obtained during cystoscopy was reported as lowgrade MALT lymphoma. A bone marrow biopsy showed no involvement by lymphoma.
The tumor was staged as IAE, and the patient received radiation therapy to the bladder and pelvis (35 Gy in 20 fractions).
Treatment was completed in September 1993. She has been followed regularly every 3 months since and was last seen in October 1998 with no evidence of recurrence.
Case 3
In October 1996, a 72-year-old woman was referred for consideration and management of recurrent urinary tract infection.
Multiple urine cultures revealed E coli infection. Two and a half
years previously, she developed nocturia 4 or 5 times nightly, and
microscopic hematuria was detected. Despite multiple courses of
antibiotics, her symptoms persisted and she subsequently developed gross hematuria. At cystoscopy, a biopsy revealed lowgrade malignant lymphoma of MALT type. On examination, no
lymphadenopathy was detected, and the chest and abdomen
were unremarkable. The patient’s tumor was staged with computed tomographic scan of the abdomen and pelvis, bone scan,
and chest radiography. Gallium scan suggested some focal areas
of increased uptake that were possibly compatible with adenopathy; however, computed tomographic scan of the abdomen did
not reveal adenopathy. The tumor was staged as IAE. The patient
Arch Pathol Lab Med—Vol 125, March 2001
Stage
Treatment
Follow-up, y
IAE
IAE
IAE
IAE
Radiation
Radiation
Radiation
Radiation
13
5
3
2
was treated with radiotherapy (35 Gy in 20 fractions) to the bladder and pelvis. She was monitored with cystoscopy every 6
months. She was last seen in March 1999 and had no evidence
of recurrence.
Case 4
A 62-year-old man presented in July 1997 with hematuria and
urgency. Urine culture revealed Staphylococcus aureus infection. At
cystoscopy, a 4-cm pedunculated tumor was seen in the bladder.
Biopsy revealed low-grade, B-cell malignant lymphoma of MALT
type. Bone marrow biopsy was negative. Computed tomographic
scan of the thorax, abdomen, and pelvis were negative except for
the presence of the mass on the left posterolateral wall of the
bladder. The tumor was staged as IAE, and the patient was treated with radiotherapy to the bladder and pelvis (35 Gy in 20
fractions). He was last seen in August 1999 with no evidence of
recurrence.
PATHOLOGIC FINDINGS
Review of the biopsies from these 4 cases showed the
classic histologic pattern of a low-grade MALT lymphoma,
including the first case, which had been initially diagnosed as lymphocytic lymphoma. Monomorphic infiltrates
of centrocyte-like cells, monocytoid cells, and/or small
lymphocytes with plasmacytoid differentiation were noted (Figure 1). Focal lymphoepithelial lesions were seen in
the biopsies of cases 2 and 4, and in both cases the involvement was restricted to areas of cystitis glandularis
(Figure 2). Reactive germinal centers were also seen in
cases 1 and 2. No evidence of transformation was seen in
any of the specimens. No muscularis propria was seen in
the biopsies, except in specimen 4, which showed infiltration by lymphoma. Plasmacytoid differentiation was seen
in all of these cases, but was more marked in case 4 with
Russell body formation.
Peripheral blood cell count at presentation was unremarkable in patients 1, 3, and 4. Patient 2 showed leukocytosis with an increased neutrophil count. No absolute
lymphocytosis was detected in any of the 4 patients.
Immunophenotyping
Light-chain restriction was demonstrated in 3 cases (cases 2, 3, and 4). Results are summarized in Table 2. Flow
cytometric data were available for case 4 and showed typical marginal zone B-cell immunophenotype (positive for
CD45 and CD20, negative for CD5, CD23, and CD10) with
k light-chain restriction and an S phase of 1%, which is
consistent with a low-grade lymphoma.
PCR for Immunoglobulin Heavy-Chain Gene
Polymerase chain reaction analyses (Figure 3) revealed
clonal immunoglobulin heavy-chain (IgH) gene rearrangement in 3 cases (cases 1, 2, and 4); PCR was not informative in case 3. Immunohistochemistry, however, showed
k light-chain restriction as well as a heavy-chain restriction in this case.
Low-Grade B-Cell Lymphoma of MALT Type—Al-Maghrabi et al 333
Figure 3. Case 4. B-cell–specific polymerase chain reaction using
primers directed at the framework 256 (FR256) regions of the immunoglobulin heavy-chain gene (IgH). The top arrow represents the internal control that is used to ensure the presence of amplifiable DNA
in each sample. The bracket in the FR256 figure denotes the size range
in which IgH gene products can be seen. Although the DNA is degraded and the signal is weak, patient B (case 4) clearly shows the
presence of a clonally rearranged IgH gene using the FR256 primers.
Clonal rearrangements of IgH genes were also noted in cases 1 and 2
(not shown in figure). Lanes A and C are from cases unrelated to this
article.
Figure 1. Case 2. Mucosa-associated lymphoid tissue lymphoma involving the lamina propria of the urinary bladder (hematoxylin-eosin,
original magnification 3100).
Figure 2. Case 2. Focal lymphoepithelial lesions in area of cystitis
glandularis (hematoxylin-eosin, original magnification 3400).
COMMENT
The incidence of secondary involvement of the urinary
bladder in lymphoma is about 13%,29 whereas primary
malignant lymphoma of the urinary bladder is an uncommon neoplasm.30–44 It accounts for 0.2% of all cases of extranodal lymphoma in North America.1 In a literature
search, Simpson et al45 identified 66 cases of primary bladder lymphoma and concluded that such cases generally
have a good prognosis. The same conclusion of favorable
prognosis was reported by Ohsawa et al,46 who also noted
that the age of patients at diagnosis ranged from 20 to 85
years (median age 64 years), with a striking female predominance (male-female ratio, 1–1.8:3). Where race was
stated, most of the patients were described as white or
Caucasian.45 The most common presenting symptoms
were hematuria followed by dysuria or nocturia.46 The
vast majority of the cases were non-Hodgkin lymphomas
of B-cell type, and among them 14% were called follicular
lymphoma. Siegelbaum et al47 noted that the majority of
these tumors were low grade and had a good prognosis.
Simpson et al45 were among the first to raise the possibility of a lower urinary tract lymphoma being of MALT
type. Although many case reports describe histologic features that are typically seen in MALT lymphoma, the first
case report of MALT lymphoma of the urinary bladder
was described by Kuhara et al.20 Since that case was described, there have been at least 17 cases of bladder MALT
lymphoma reported in the literature.2,19,21–24 All except 2 of
the 17 cases were of low grade.22 Generally the prognosis
was very good. Pawade et al2 described 5 cases of MALT
lymphoma that arose in the urinary bladder. Four were in
women, and one in a man. One case remained untreated
for 8 years. These authors found lymphoepithelial lesions
in 1 case, which was the only case showing cystitis glan-
Table 2. Immunohistochemical and Polymerase Chain Reaction (PCR) Findings*
Case No.
CD45
CD20
CD45RO
CD5
CD10
CD43
K&L
PCR
1
1
1
I
ND
ND
2
I
Monoclonal
2
1
1
2
2
2
2
LLCR
Monoclonal
3
1
1
2
2
2
2
KLCR
I
4
1
1
2
2
2
F1
KLCR
Monoclonal
* Plus sign indicates positive reaction; I, inconclusive; minus sign, negative reaction; ND, not done; F1, focally positive; LLCR, l-light chain
restriction; and KLCR, k-light chain restriction.
334 Arch Pathol Lab Med—Vol 125, March 2001
Low-Grade B-Cell Lymphoma of MALT Type—Al-Maghrabi et al
dularis. In a review of the Mayo Clinic records for the last
56 years, Kempton et al21 reported 6 cases of primary bladder lymphoma, all of which were considered of MALT
type, stage IAE, and all of which received radiotherapy
with or without surgery. No patient had recurrent lymphoma or died of lymphoma.
Lymphoepithelial lesions have been described only in
the areas of cystitis glandularis in the cases described by
Pawade et al and Kempton et al. We found focal lymphoepithelial lesions in 2 cases, and in both they were also
restricted to areas of cystitis glandularis. The rarity of
lymphoepithelial lesions in MALT lymphoma of the urinary bladder and the confinement to the areas of cystitis
glandularis and cystitis cystica suggest that the transitional epithelium is resistant to invasion by lymphoma cells.
Thus, the presence of lymphoepithelial lesions is not mandatory for the diagnosis of MALT lymphoma of the bladder if there are other features typical of MALT lymphomas.
No molecular findings have been reported in previously
reported studies of bladder lymphomas. In our cases, IgH
gene rearrangement was present in 3 of 4 cases, thus PCR
analysis should be useful in the differential diagnosis of
chronic cystitis.
Most MALT lymphomas arise in extranodal sites in the
setting of acquired MALT.48 In these sites, acquired MALT
could be induced by Helicobacter pylori infection in the
stomach49–51 or by autoimmune diseases, such as Sjögren
syndrome in salivary glands7 or Hashimoto disease in the
thyroid gland.14 Since there is no naturally occurring lymphoid tissue in the bladder, it is possible that preexisting
chronic inflammation can induce acquired MALT. Simpson et al45 found that 22% of patients had a history of
chronic cystitis, but in most cases convincing histologic
evidence of long-standing inflammation was lacking. Ohsawa et al46noted in his review that 20% of patients with
primary lymphoma of the urinary bladder had a history
of chronic cystitis. Owing to the relatively low percentage
of patients with a history of chronic cystitis, some authors
have agreed that primary bladder lymphomas are not of
the MALT type. The incidence of chronic cystitis may be
underestimated. All our patients had a history of chronic
cystitis, and most of the recently described cases have the
same history.2,21 Escherichia coli infection was found in 3 of
our patients; however, we cannot conclude any positive
correlation from this small number. The other less likely
possible origin of MALT arises from the fact that the bladder is an embryogenic derivative of the cloaca, and the
bladder lymphoma might arise from inherent lymphoid
tissue that is related to Peyer patches in the gut. Most studies, however, have failed to identify lymphoid tissue in
healthy bladder.22 Luppi et al52 demonstrated the presence
of hepatitis C virus RNA in 8 of 16 patients with MALT
lymphoma of different sites and suggested hepatitis C virus as a potential infectious cofactor in the pathogenesis
of MALT lymphoma; however, the relation of hepatitis C
virus infection and bladder MALT lymphoma has not
been established.
All our patients’ tumors were stage IAE, and all were
managed with radiotherapy alone. All the patients were
in complete remission at the time this article was written,
with follow-up periods of 13 years, 5 years, 3 years, and
2 years. We conclude that MALT lymphoma of bladder is
more common in women, potentially as a result of increased incidence of chronic cystitis in women. Primary
Arch Pathol Lab Med—Vol 125, March 2001
bladder lymphomas are usually low grade and remain localized with a favorable prognosis, although the literature
contains 2 reported cases22 showing transformation to a
diffuse large cell lymphoma. Molecular studies are very
useful in confirming the diagnosis by demonstration of
monoclonality, especially in small biopsies in which the
morphologic examination is not diagnostic alone. Local radiotherapy appears to result in excellent control of the
disease.
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