DOI:10.2214/AJR.07.2629
AJR 2008; 191:921-930
© American Roentgen Ray Society
Marginal Zone B-Cell Non-Hodgkin's Lymphoma of Mucosa-Associated Lymphoid Tissue Type: Imaging Findings
Olga Maksimovic1,
Wolfgang A. Bethge2,
Jan P. Pintoffl2,
Monika Vogel1,
Claus D. Claussen1,
Roland Bares3 and
Marius Horger1
1 Department of Diagnostic Radiology, Eberhard-Karls-University,
Hoppe-Seyler-Strasse 3, 72076 Tübingen, Germany.
2 Department of Internal Medicine–Oncology, Eberhard-Karls-University,
Tübingen, Germany.
3 Department of Nuclear Medicine, Eberhard-Karls-University, Tübingen,
Germany.
Received May 25, 2007;
accepted after revision July 23, 2007.
Address correspondence to M. Horger
(mshorger{at}med.uni-tuebingen.de).
Abstract
OBJECTIVE. The aim of this essay is to describe the imaging features
of marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue
(MALT) type throughout various organs.
CONCLUSION. Awareness of the expected locations of MALT lymphoma
combined with knowledge of the incidence and imaging findings leads to
accurate diagnosis of lesions suspicious for this disorder and helps to
differentiate this disease from other abnormalities.
Keywords: lymphoma imaging • MALT lymphoma • marginal zone B-cell non-Hodgkin's lymphoma • mucosa-associated lymphoid tissue type
Introduction
The three types of marginal zone B-cell non-Hodgkin's
lymphoma—splenic, nodal, and mucosa-associated extranodal—are each
distinct clinicopathologic entities. Mucosa-associated lymphoid tissue (MALT)
neoplasms constitute approximately 5% of all non-Hodgkin's lymphomas
[1]. Systemic B symptoms are
uncommon with MALT lymphoma, and there is a rare (< 25% of cases)
association with nodal or medullar involvement. Moreover, peripheral blood
usually is not initially involved. Because MALT lymphoma originates most
frequently in various extranodal sites, approximately 51% of cases being in
the gastrointestinal tract, diagnosis is challenging. Additional potential
primary sites are the orbit and ocular adnexa, lung, skin, soft tissues,
parotid gland, thyroid gland, thymus, Waldeyer's tonsillar ring, breast, and
pancreas [2]. Results of
epidemiologic studies suggest a strong association between gastric and even
extragastric MALT lymphoma and chronic Helicobacter pylori infection
[3]. Autoimmune diseases also
are predisposing disorders for MALT lymphoma. MALT lymphoma tends to remain
localized in the affected organ for a prolonged period, being indolent and
therefore responding well to therapy
[2]. These lymphomas, however,
can progress to high-grade large B-cell lymphoma
[2].
Ocular Adnexal MALT Lymphoma
MALT lymphoma represents approximately 50% of all ocular adnexal lymphomas
[3]. Ocular adnexal MALT
lymphoma localizes primarily in the conjunctiva, lacrimal glands, orbit, and
eyelids, unlike high-grade lymphoma, which localizes mainly in the intraocular
region [4]. Imaging findings
include diffuse infiltration of the ocular adnexa with homogeneous attenuation
and strong contrast enhancement on CT or MRI
(Fig. 1). The MRI findings
generally reveal homogeneously high signal intensity on T2-weighted
fat-saturated images and correspondingly intermediate or slightly low signal
intensity on T1-weighted images. Among the differential diagnoses of ocular
adnexal MALT lymphoma, idiopathic orbital inflammatory pseudotumor is the most
challenging. On CT, however, orbital inflammatory pseudotumor displays no
specific attenuation values. On MRI, signal intensity depends on the degree of
fibrosis, low signal intensity sometimes being present on T2-weighted images
[5].
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Fig. 1 —59-year-old woman with mucosa-associated lymphoid tissue
lymphoma of ocular adnexa. Axial contrast-enhanced CT scan shows enlargement
and asymmetry of right lacrimal gland (arrow) extending into
retrobulbar space, presenting diffuse strong enhancement. Differential
diagnosis should exclude inflammatory pseudotumors of orbit, benign
lymphoproliferation, pseudolymphoma, and other orbital neoplasms.
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MALT Lymphoma of the Parotid Gland
Primary lymphoma in a salivary gland is an unusual finding that accounts
for 4.7% of lymphomas at all sites
[6]. Despite an increased
incidence of MALT lymphoma in association with Sjögren's syndrome, most
salivary gland lymphomas occur without this autoimmune disorder. CT of MALT
lymphoma of the parotid gland reveals swelling of the superficial lobe and
sometimes multiple calcifications disseminated throughout the gland
(Fig. 2). Furthermore, multiple
hypoattenuating solid nodules, which correspond to hyperplastic lymphoid
tissue or lymphoma, can be observed. Cystic lesions may coexist, representing
cysts arising from compression of terminal parotid ducts by contiguous
hyperplastic or neoplastic lymphoid tissue. In patients with Sjögren's
syndrome, small foci of high signal intensity on MRI represent focal
dilatation of salivary ducts or cysts, which is frequent in this disorder
[2] (Fig.
3A,
3B,
3C). Secondary involvement of
MALT lymphoma is easily visualized as asymmetric hyperattenuating soft-tissue
infiltration of physiologically hypodense glands.
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Fig. 2 —49-year-old woman with newly diagnosed mucosa-associated
lymphoid tissue (MALT) lymphoma of right parotid gland. Contrast-enhanced
axial CT scan shows high attenuation of right parotid gland (arrow).
Poor definition of glandular borders is caused by lymphoma infiltration
extending into retromandibular space and along main parotid duct. In patients
with primary MALT lymphoma of parotid gland without coexistent Sjögren's
syndrome, typical imaging finding is focal nodular or diffuse unilateral or
bilateral parenchymal infiltration with increased attenuation and contrast
enhancement.
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Fig. 3A —57-year-old woman with Sjögren's syndrome and associated
mucosa-associated lymphoid tissue (MALT) lymphoma of parotid gland. Left
parotid gland was resected several years previously because of MALT lymphoma.
Coronal CT reformation after IV administration of contrast material shows
enlargement and induration of contralateral gland (arrow).
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Fig. 3B —57-year-old woman with Sjögren's syndrome and associated
mucosa-associated lymphoid tissue (MALT) lymphoma of parotid gland. Left
parotid gland was resected several years previously because of MALT lymphoma.
T2-weighted coronal MR image shows swelling of right parotid gland and
dilatation of salivary ducts or cysts (arrow). Changes were caused by
ductal epithelial proliferation with obliteration of ductal lumina in
late-stage Sjögren's syndrome.
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Fig. 3C —57-year-old woman with Sjögren's syndrome and associated
mucosa-associated lymphoid tissue (MALT) lymphoma of parotid gland. Left
parotid gland was resected several years previously because of MALT lymphoma.
T1-weighted coronal MR image shows MALT lymphoma involvement (arrow)
of parotid gland responsible for progressive soft-tissue infiltration and
gadolinium enhancement manifesting as honeycombing. Differentiation of benign
lymphoepithelial lesions of parotid gland from MALT lymphoma infiltration
requires extensive sampling and immunochemical analysis. In AIDS patients,
MALT lymphoma can accompany benign lymphoepithelial lesions.
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MALT Lymphoma of the Skin
Cutaneous and subcutaneous involvement of MALT lymphoma is rare (Figs.
4A,
4B,
4C and
5). Imaging shows focal
plaquelike or diffuse cutaneous infiltration
[7]. In time, MALT lymphoma of
the skin may develop calcifications (Fig.
4C). Although rare, multifocal involvement is common in these
patients (Fig. 5). As in MALT
lymphoma in other locations, imaging reveals homogeneous attenuation and mild
contrast enhancement on CT scans, intermediate to low signal intensity on
T1-weighted MR images, and intermediate to slightly increased signal intensity
on T2-weighted MR images.
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Fig. 4A —59-year-old woman with multifocal cutaneous and subcutaneous
involvement of mucosa-associated lymphoid tissue (MALT) lymphoma. Axial
contrast-enhanced CT scan of cervical region shows plaquelike infiltration
(arrow) of platysma muscle.
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Fig. 4B —59-year-old woman with multifocal cutaneous and subcutaneous
involvement of mucosa-associated lymphoid tissue (MALT) lymphoma. Axial
contrast-enhanced CT scan shows focal MALT lymphoma infiltration extending
over left maxilla and levator angulus oris muscle (arrow).
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Fig. 4C —59-year-old woman with multifocal cutaneous and subcutaneous
involvement of mucosa-associated lymphoid tissue (MALT) lymphoma. Axial
contrast-enhanced CT scan shows masslike MALT lymphoma infiltration
(arrows) extending along posterior fascia of trapezius muscle, which
is not sharply delineated. Calcifications within tumor are evident. Findings
resemble those of dermatomyositis.
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Fig. 5 —82-year-old woman with histologically proven
mucosa-associated lymphoid tissue lymphoma. Axial contrast-enhanced CT scan
shows ill-defined star-shaped infiltration (arrows) of gluteal region
on both sides and spreading along gluteus maximus muscular fascia. Changes can
be easily misinterpreted as hematoma or panniculitis.
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MALT Lymphoma of the Lung
Primary pulmonary lymphoma is an uncommon neoplasm, the prevalence being
less than 1%. It is generally classified as MALT lymphoma or
bronchus-associated lymphoid tissue lymphoma and is a well-known manifestation
of extranodal marginal zone lymphoma
[8]. The various patterns of
pulmonary involvement are nodules, single or multiple localized areas of
consolidation usually with an accompanying air bronchogram, peribronchial
infiltrates, and reticulation (Figs.
6,
7,
8). Little change in size or
morphologic features of the lesion over a prolonged period suggests indolence
and helps to differentiate this lesions from other pathologic entities,
particularly infection. 18F-FDG PET uptake in bronchus-associated
lymphoid tissue lymphoma is usually mild and is not a factor that
differentiates the lesion from other pulmonary disorders, including infection
[9]
(Fig. 9).
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Fig. 6 —62-year-old woman with histologically proven
mucosa-associated lymphoid tissue lymphoma of lung. Axial high-resolution CT
scan shows rare form of pulmonary involvement manifesting as generalized
septal thickening, reticulation, and moderate ground-glass opacity. Pattern of
pulmonary infiltration mimics fibrosis or alveolar proteinosis.
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Fig. 7 —58-year-old woman with mucosa-associated lymphoid tissue
lymphoma of lung. CT scan shows multifocal pulmonary areas of ground-glass
opacity and, especially, consolidation, which are in part ill-defined and
centered by subsegmental bronchia (arrows). Imaging features and slow
kinetics of these pulmonary infiltrates are difficult to differentiate from
those of bronchoalveolar carcinoma and nodular amyloidosis.
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Fig. 8 —78-year-old man with histologically proven mucosa-associated
lymphoid tissue (MALT) lymphoma of lung. CT scan shows focal nodular mass
representing MALT lymphoma. Discrete positive airspace bronchogram is evident.
Differential diagnoses include nodular lymphoid hyperplasia, Wegener's
granulomatosis, and cryptogenic interstitial pneumonia.
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Fig. 9 —56-year-old man with mucosa-associated lymphoid tissue (MALT)
lymphoma of lung. Coronal reformation of whole-body FDG PET scan shows
discrete focal uptake in nodular MALT lymphoma (arrow) of right lung.
Average standard uptake value was 1.3, which allows no further differentiation
from infection, inflammation, or benign lung tumor.
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MALT Lymphoma of the Biliary Tract
Involvement of the biliary tract by MALT lymphoma is extremely rare.
Infiltration of intrahepatic and extrahepatic ducts and of the gallbladder
causes segmental or diffuse wall thickening usually without stenosis or
jaundice. On CT and sonography, the layers of the gallbladder wall are ill
defined, and contrast enhancement is only moderate (Fig.
10A,
10B).
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Fig. 10A —62-year-old woman with mucosa-associated lymphoid tissue
lymphoma involving gallbladder. Contrast-enhanced CT scan shows massive
thickening of gallbladder wall (arrow) due to lymphoma.
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Fig. 10B —62-year-old woman with mucosa-associated lymphoid tissue
lymphoma involving gallbladder. Subcostal conventional B-mode sonogram shows
gallbladder wall thickening (arrow) up to 8 mm thick
(asterisks) predominantly in fundal region. Unlike findings in
gallbladder carcinoma, all wall layers of gallbladder are preserved.
Differentiation from adenomyomatous hyperplasia can prove difficult and relies
mainly on visualization of small cystic spaces (Rokitansky-Aschoff sinuses)
and concretions apparent on sonograms and T2-weighted MR images.
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MALT Lymphoma of the Gastrointestinal Tract
The gastrointestinal tract, particularly the stomach, is the most common
primary site of MALT lymphoma
[1]. In decreasing order of
frequency, other gastrointestinal sites involved are the ileocecal tract,
colon, rectum, duodenum, and esophagus
[1]. Because no lymphoid tissue
is found in the gastric mucosa, the occurrence of gastric MALT lymphoma has
been linked to follicular gastritis caused by H. pylori, probably in
response to a chronic inflammatory stimulus. Common CT findings in gastric
MALT lymphoma are severe or moderate, diffuse or segmental wall thickening and
minimal to moderate contrast enhancement. Sometimes, however, mucosal
nodularity, shallow ulcer, and severe fold thickening and circumferential
growth with diffuse rugal enlargement caused by submucosal spread of the tumor
are seen [10] (Figs.
11A,
11B and
12A,
12B). The last feature,
however, is considered more suggestive of gastric carcinoma. Independently of
extent of lymphoma infiltration, the stomach usually remains pliable and
distensible without marked narrowing of the lumen.
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Fig. 11A —56-year-old man with gastric mucosa-associated lymphoid
tissue (MALT) lymphoma. Coronal reformation of abdominal contrast-enhanced CT
scan shows circular growth of MALT lymphoma (small arrow) at gastric
angle. Nodal involvement (large arrows) also is evident.
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Fig. 11B —56-year-old man with gastric mucosa-associated lymphoid
tissue (MALT) lymphoma. CT scan shows circular growth of MALT lymphoma
(arrow) at gastric angle mimicking carcinoma. As with most
gastrointestinal lymphomas, there is no luminal stenosis.
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Fig. 12A —80-year-old man with gastric mucosa-associated lymphoid
tissue (MALT) lymphoma. CT scan shows strong segmental wall thickening in
fundus and body of stomach. Contrast enhancement (arrow) along lesser
curvature changes owing to lymphoma infiltration.
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Fig. 12B —80-year-old man with gastric mucosa-associated lymphoid
tissue (MALT) lymphoma. Contrast-enhanced CT scan shows polypoid multifocal
gastric wall thickening along greater curvature with moderate contrast
enhancement (arrow). At macroscopic inspection, low-grade MALT
lymphoma usually exhibits multiple instances of superficial spreading of
lesions without ulceration, whereas high-grade lymphoma exhibits solitary
tumor-forming lesion. Shallow ulcer usually indicates high-grade lymphoma or,
more commonly, gastric carcinoma.
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Unlike gastric involvement, involvement of the duodenum alone is rare in
MALT lymphoma and generally is associated with other gastrointestinal
manifestations of the disease (Fig.
13A,
13B). Small-intestinal
involvement in MALT lymphoma usually consists of solitary lesions, but in
10–25% of cases, multiple sites are affected. The distal ileum is
primarily affected, possibly because of the greater amount of lymphoid tissue
in this part of the bowel. The bulk of the tumor is located in the intestinal
wall. Circumferential tumors characteristically affect relatively long
segments of bowel. Submucosal tumor infiltration can cause effacement of
mucosal folds, often producing a smooth, featureless appearance within the
involved segment (Fig. 14A).
Obstruction is uncommon because the infiltrating tumor weakens the muscularis
propria and does not elicit a desmoplastic response
[1]. The colon is a much less
common site of MALT lymphoma, which preferentially involves the cecum or
rectum (Fig. 14B)
[1]. The lesions can be
polypoid, infiltrative, or cavitary (Fig.
14C). The infiltrative form is characterized by a long segment of
concentric narrowing with smooth overlying mucosa and thickened, irregular
haustral folds caused by submucosal tumor infiltration.
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Fig. 13A —62-year-old woman with duodenal mucosa-associated lymphoid
tissue lymphoma. Axial contrast-enhanced CT scan shows segmental circular wall
thickening (arrow) in duodenum. Definition of mucosa and submucosa is
poor owing to diffuse lymphoma infiltration.
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Fig. 13B —62-year-old woman with duodenal mucosa-associated lymphoid
tissue lymphoma. Subcostal conventional B-mode sonogram shows duodenal wall
thickening with good delineation of all mural layers (arrow).
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Fig. 14A —70-year-old man with histologically proven gastrointestinal
mucosa-associated lymphoid tissue (MALT) lymphoma with involvement of stomach,
mesentery, and colon. T2-weighted turbo spin-echo (TR/TE, 4,260/95) MR image
shows diffuse moderate thickening (arrow) of intestinal wall. As
expected, luminal stenosis is not present. Small-intestinal MALT lymphoma
usually is preceded by immune proliferative small-intestinal disease.
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Fig. 14B —70-year-old man with histologically proven gastrointestinal
mucosa-associated lymphoid tissue (MALT) lymphoma with involvement of stomach,
mesentery, and colon. Axial contrast-enhanced CT scan shows right colonic wall
thickening (large arrow) with infiltration of adjacent greater
omentum (small arrow). Morphologic features are difficult to
differentiate from those of carcinoma with peritoneal spread.
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Fig. 14C —70-year-old man with histologically proven gastrointestinal
mucosa-associated lymphoid tissue (MALT) lymphoma with involvement of stomach,
mesentery, and colon. CT scan shows severe rectal wall thickening
(arrow) due to MALT lymphoma infiltration.
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MALT Lymphoma of the Breast
In the literature, MALT lymphoma constitutes a variable subgroup of
0–44% of all types of breast lymphoma
[11]. Mammography has shown
unilateral diffuse involvement and bilateral diffuse involvement or solitary
or multiple masses with irregular or partly defined or well-defined borders.
On contrast-enhanced breast MRI, lymphomas have been visualized as
hyperintense on T2-weighted images and isointense on T1-weighted images with
strong and rapid contrast enhancement
[12]. CT usually shows
homogeneous attenuation and only moderate enhancement of well-margined
masslike lesions (Figs. 15 and
16). Doppler sonography,
however, reveals heterogeneity and strong vascularization of MALT
lymphoma.
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Fig. 15 —79-year-old woman with bilateral histologically proven
mucosa-associated lymphoid tissue lymphoma of breast. CT scan shows bilateral
well-marginated breast masses (arrows) with homogeneous attenuation.
Differentiation from other rare tumors, such as phyllodes tumor, is difficult
and requires biopsy.
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Fig. 16 —78-year-old woman with mucosa-associated lymphoid tissue
(MALT) lymphoma of breast. CT scan shows solitary breast involvement by MALT
lymphoma (arrow) evidenced by homogeneous low-attenuation mass with
mild contrast enhancement. Mild to moderate CT attenuation in breast
parenchyma results from short delay time used for chest imaging with
whole-body investigation protocols. Delayed CT scans show progressive
enhancement.
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Waldeyer's Tonsillar Ring MALT Lymphoma
MALT lymphoma has been found in the palatine and lingual tonsils, nasal
mucosa, and base of the tongue
[13]. Submucosal tumor
infiltration usually obliterates normal landmarks in the pharynx. Swelling and
a homogeneously attenuating mass are typical findings (Fig.
17A,
17B).
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Fig. 17A —80-year-old man with mucosa-associated lymphoid tissue (MALT)
lymphoma involving tonsils. Axial contrast-enhanced CT scan of cervical region
shows involvement of Waldeyer's tonsillar ring by MALT lymphoma. Arrow
indicates right palatine tonsil.
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Fig. 17B —80-year-old man with mucosa-associated lymphoid tissue (MALT)
lymphoma involving tonsils. CT scan shows infiltration of right lingual tonsil
(arrow). Use of 18F-FDG PET for differentiation from
high-grade tonsillar lymphoma or carcinoma can prove beneficial because low
tracer avidity is expected only in low-grade lymphoma, including MALT lymphoma
(not shown). Diffusion-weighted imaging seems useful for differentiating tumor
and nontumorous masses and even for establishing biologic aggressiveness of
tumors reflected by different cellularities and macromolecular interactions.
Apparent diffusion coefficient (ADC) measurement with diffusion-weighted
imaging may be useful in differentiation of extranodal lymphoma and carcinoma.
Low ADC values are characteristic of malignant lymphoma in head and neck and
other locations.
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Conclusion
For accurate staging, awareness of the potential sites of primary
involvement of extranodal MALT lymphoma and the patterns of infiltration and
spread toward another MALT-containing organs according to the homing
phenomenon is essential. Adjunctive use of functional imaging techniques, such
as FDG PET/CT, somatostatin receptor scintigraphy, and diffusion-weighted MRI,
can be beneficial for staging and especially for assessment of therapeutic
response (Fig. 18A,
18B)
[14,
15].
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Fig. 18A —58-year-old man with mucosa-associated lymphoid tissue (MALT)
lymphoma with additional nodal involvement at follow-up. Fusion FDG PET/CT
scan shows focal nodal uptake (average standard uptake value, 3.4) in
paracardial mass (arrow).
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Fig. 18B —58-year-old man with mucosa-associated lymphoid tissue (MALT)
lymphoma with additional nodal involvement at follow-up. Fusion FDG PET/CT
scan 6 weeks after institution of chemotherapy shows marked reduction in FDG
uptake (arrow) accompanying tumor shrinkage. Use of FDG PET is
especially beneficial to patients with MALT lymphoma and plasmacytic
differentiation ( 30% of all MALT lymphomas) because of higher avidity for
FDG in this group. As is FDG PET, whole-body diffusion-weighted MRI for survey
of nodal involvement by MALT lymphoma should be considered as an alternative
functional imaging technique.
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Abstract
Introduction
