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Thomas et al.
Extranodal Lymphoma CME Extranodal Lymphoma From Head to Toe
SAM
Nuclear Medicine and Molecular Imaging
Review
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L
ymphoma is a relatively common renchyma, cavitating lung nodules, persistent
malignancy affecting all ages, but consolidation, widespread pulmonary nodu
it predominantly affects those in larity, and reticular patterns with interlobular
later life. Like various other con septal thickening have been reported [4].
ditions, such as tuberculosis, lymphoma is The differential diagnosis is particular
known as a “great imitator” and should be ly difficult given the spectrum of coexis
considered when mass lesions are seen any tent pulmonary diseases in this cohort of pa
where in the body. This review will continue tients. Interstitial change may be related to
the discussion of the imaging manifestations drug reactions from chemotherapy regimes,
of extranodal lymphoma that began in part 1 cavitating nodules may represent atypical in
[1] by focusing on the imaging manifestations fections, and widespread nodularity is seen
of extranodal lymphoma in the trunk and ex in bone marrow transplant recipients with
tremities. The imaging modalities and find posttransplant lymphoproliferative disorder.
ings that best allow differentiation of lympho Pleural effusions are commonly seen in as
ma from other differential diagnoses will also sociation with pulmonary lymphoma but tend
be considered. to be reactive and only rarely contain malig
nant cells in the absence of pleural masses.
Thorax The prevalence of nonmalignant pleural effu
Keywords: CT, extranodal lymphoma, MRI, non-Hodgkin Nodal involvement in the chest is common sions is thought to be secondary to proximal
lymphoma
in both Hodgkin disease and non-Hodgkin lymphatic obstruction from the underlying
DOI:10.2214/AJR.11.6738 lymphoma (NHL). The site of nodal enlarge nodal disease. The same cannot be said for
ment may be suggestive of the diagnosis— pericardial effusions, which are usually ma
Received June 14, 2010; accepted after revision with Hodgkin disease involving the ante lignant when seen in association with lym
January 20, 2011. rior mediastinal nodes and NHL involving phoma [5]. Cardiac involvement is thought to
1
All authors: Department of Radiology, University
the subcarinal, paraesophageal, and internal be common (up to 24%) but underrecognized
Hospitals of Leicester NHS Trust, Leicester General mammary nodes—but is by no means spe on standard imaging protocols [6].
Hospital, Gwendolen Rd, Leicester, Leicestershire cific in distinguishing between the two enti The chest wall may be involved in aggres
LE5 4PW, United Kingdom. Address correspondence to ties [2] (Fig. 1). The thymus is regarded as a sive disease, usually in association with exten
A. Rajesh (arajesh27@hotmail.com).
nodal station with regard to staging [3]. sive intrathoracic disease. Primary lympho
CME/SAM Lung parenchymal involvement is more matous masses in the breast are exceedingly
This article is available for CME/SAM credit. common as part of disseminated Hodgkin dis rare, with an incidence of 0.75% of breast
See www.arrs.org for more information. ease than NHL, but primary pulmonary lym lumps. The breast may be involved as an ex
phoma (i.e., without evidence of significant tranodal site in 1–2% of cases of systemic
AJR 2011; 197:357–364
nodal disease) is more commonly NHL (Figs. lymphoma; again, NHL predominates [7].
0361–803X/11/1972–357 2 and 3). The patterns of pulmonary involve Secondary involvement of the breast in NHL
ment in either disease are many and varied. is more common and may manifest as diffuse
© American Roentgen Ray Society Extension of hilar nodal masses into lung pa skin thickening seen on mammography [8].
Fig. 1—38-year-old man with night sweats and weight loss. Fig. 2—58-year-old woman who presented with
A and B, Fused PET/CT images, coronal reconstruction (A) and axial source image (B), show marked uptake in shortness of breath and weight loss. Radiograph
right paracardiac mass (arrows). Mediastinal masses may represent conglomerates of lymph nodes, thymic shows bilateral parenchymal alveolar opacification
masses, or diffuse mediastinal soft-tissue extranodal spread. Solid nature of mass excludes foregut duplication (arrows). Although opacification appears masslike,
cyst, and there is no connection to pericardium to suggest pericardial cyst or defect in this case. CT-guided bilateral perihilar alveolar shadowing can be caused
biopsy in this case revealed diffuse large B-cell lymphoma. by pulmonary edema, drug-induced changes, or
atypical infection. Imaging appearances are not
specific for lymphoma in this case. Postmortem
Upper Abdominal Solid Organs lignancy to affect the spleen [11]. Appear findings in this case revealed diffuse alveolar
As in other parts of the body, the most ances may be subtle with only homogeneous anaplastic lymphoma.
common form of lymphoma in the abdom enlargement to suggest infiltration. Multipla
inal cavity involves widespread lymphade nar reformations of cross-sectional CT may
nopathy that may be paraaortic or may extend be helpful in measuring splenic size, but a as calcification or clinical features of infec
into the mesentery. Appearances on imaging sign of significant (i.e., clinically palpable) tion should also raise suspicion of a lympho
are of homogeneous, hypoechoic masses on splenic enlargement on axial images is ex matous deposit. The appearance of a solitary
ultrasound. CT shows homogeneous soft- tension of splenic tissue below the left cos splenic mass in a patient with previously di
tissue–density masses in the distribution of tal margin. Solitary splenic masses have also agnosed low-grade lymphoma should raise
known nodal chains and locations. Nodal been reported in cases of lymphoma and are the suspicion of high-grade transformation
masses may form out of a conglomeration usually of low attenuation in relation to the particularly if there are aggressive features
of multiple enlarged nodes. Calcification of surrounding spleen on enhanced CT (Fig. 5). such as capsular breach [9].
lymph nodes in lymphoma is usually seen Other features such as associated adenopathy Normal nodal tissue surrounds the pancreas,
only after treatment [9]. Involvement of the and absence of nonaggressive features such and because small low-attenuation pancreatic
solid abdominal viscera may be seen in com
bination with nodal disease or may be seen
as primary extranodal disease.
Lymphomatous disease in the liver may
take various forms. Diffuse hepatic enlarge
ment, often seen in conjunction with sple
nomegaly, is common. Multiple hypodense
enhancing masses involving multiple organs
mimicking multiple metastatic deposits have
been described. Lymphoma remains on the
differential of a solitary liver deposit (Fig. 4).
Peripheral ring enhancement may be seen and
should be differentiated from fungal infection,
particularly in an immunocompromised pa
tient [4]. Finally, a periportal infiltrative pat Fig. 3—60-year-old man with known diffuse large B-cell lymphoma.
tern may be seen, particularly in association A and B, Axial contrast-enhanced CT scans of thorax on soft-tissue windows (A) and lung windows (B)
with splenomegaly in Hodgkin disease [10]. show multiple parenchymal soft-tissue masses (arrows). Patient did not respond to antibiotic therapy, which
As with the liver, the spleen is common prompted biopsy of two areas of persistent consolidation. Biopsy findings confirmed pulmonary involvement
by diffuse large b-cell lymphoma. Pulmonary involvement in patients with lymphoma can be difficult to
ly involved in abdominal lymphoma; indeed, differentiate from atypical infection and drug reactions. Imaging appearances in this case were not specific for
lymphoma is the most common primary ma lymphoma over other differential possibilities.
Fig. 4—55-year-old man with itching, weight Fig. 5—39-year-old man with deranged liver function Fig. 6—45-year-old man with generalized abdominal
loss, and night sweats. Axial contrast-enhanced tests and weight loss. Axial contrast-enhanced pain and weight loss. Contrast-enhanced portal
portal venous phase CT image shows focal CT image of abdomen shows solitary hypodense venous phase CT image of abdomen shows
hypodense lesion (arrows) in left lobe of liver and lesion (arrow) in anterior part of spleen that later diffuse low-attenuation, poorly enhancing mass
also multiple low-attenuation lesions in spleen. disappeared after chemotherapy. Differential (white arrow) enlarging pancreas. Additional
Appearances could be caused by multiple epithelial diagnosis includes splenic metastasis, abscess, low-attenuation deposits (black arrow) are seen
metastatic deposits or even by sarcoidosis or and hemangioma. No specific features are seen on in upper pole of right kidney. Primary differential
other granulomatous conditions; however, low- imaging to suggest lymphoma, but clinical features consideration is metastatic epithelial malignancy and
attenuation nature of lesions and clinical history led to bone marrow aspiration, which revealed none of imaging features present suggest lymphoma
suggest lymphoma as primary consideration. Biopsy follicular lymphoma. as more likely diagnosis. Diagnosis of follicular
of superficial hepatic lesion revealed diffuse large lymphoma was made on bone marrow aspirate and
B-cell lymphoma. trephine biopsy.
malignancies can be difficult to detect, particu sult in adrenal insufficiency. Given the prev hyperechogenicity relative to the kidney on
larly on CT, it can be difficult to discern the ori alence of steroids in chemotherapy regimens ultrasound scanning and higher attenuation
gin of marked lymphadenopathy in this region. for lymphoma, the possibility of adrenal in relative to kidney on unenhanced CT scans.
One clue is that metastatic nodal involvement sufficiency raised by imaging features is im Renal cell carcinoma tends to be both hy
from pancreatic adenocarcinoma rarely ex portant to communicate to the clinical team. poechoic and hypoattenuating in these cir
tends below the level of the renal veins; in such Diffuse mesenteric disease in advanced cumstances [17]. Direct renal extension from
cases, a lymphoproliferative disorder should be malignancy may present a challenge to the paraaortic or retroperitoneal lymphadenopathy
suspected [9]. Direct involvement of pancre radiologist in suggesting the site of primary
atic tissue by lymphoma may be through con disease. A few clues are helpful in identifying
tiguous spread from surrounding nodal tissue lymphomatous disease. Diffuse sheetlike in
(seen in 30% of patients with NHL involving filtration of the mesentery is seen almost ex
the pancreas) or, like with the liver and spleen, clusively in NHL [14]. The sandwich sign, in
through diffuse homogeneous enlargement by which the mesenteric vessels are compressed
infiltrative lymphomatous disease [12] (Fig. 6). between nodal and soft-tissue masses with
There may be stranding of the peripancreatic out evidence of distal vascular compromise,
fat, which may be difficult to differentiate from has been described [15]. Nodular mesenter
the appearances of pancreatitis. In such cases, ic soft-tissue masses with ascites and subdia
in the absence of other nodal or extranodal dis phragmatic deposits are more suggestive of
ease, follow-up imaging is necessary to differ epithelial malignancies such as ovarian or
entiate inflammatory change from underlying colonic tumors. Even advanced disease may
malignant infiltration. show a dramatic response to therapy in lym
With the increasing use of cross-section phoma; the residual of diffuse mesenteric in
al imaging, the detection of bilateral adre volvement may be as little as a “misting” of
nal enlargement is increasingly common. the mesenteric fat on follow-up CT [9].
The cause of enlargement may be difficult
to determine. In the case of disseminat Genitourinary System
ed NHL, there is a significant chance adre The kidneys contain no intrinsic lymphoid Fig. 7—33-year-old man who presented with
abdominal pain, enlarged testicle, and diplopia.
nal enlargement may be due to lymphoma tissue, so involvement by lymphoma is usual Coronal contrast-enhanced reconstructed CT image
tous infiltration (seen in 25% of patients with ly late in the disease process and in the pres shows multiple low-attenuation, poorly enhancing
disseminated disease [9]). Other patterns ence of disseminated disease [9]. Like with cortical bilateral renal masses (arrows) in case of
disseminated diffuse mixed cell lymphoma. Medial
of involvement include focal masses or uni lymphoma of other solid abdominal organs, rectus involvement (not shown) accounted for
lateral enlargement [11, 13]. The increased both solitary or multiple focal masses (Figs. diplopia, and diffuse testicular involvement (not
use of PET in staging lymphoma patients is 6 and 7) and diffuse infiltration (Figs. 8 and shown) accounted for scrotal pain and swelling.
helpful here: Lymphomatous disease will be 9) in the kidney have been described [16]. Although diffuse infection, pyelonephritis, or
metastases could be considered, clinical features
FDG avid, whereas adrenal hyperplasia will Clues to differentiate lymphoma from oth and disseminated involvement are more suggestive
not. Sometimes the extent of disease will re er renal soft-tissue masses on imaging include of lymphoma in this case.
Fig. 12—76-year-old man who presented with weight Fig. 13—63-year-old woman who presented with
loss and anemia. Axial contrast-enhanced CT image abdominal pain and palpable abdominal mass.
shows diffuse gastric wall thickening (arrow) with Axial contrast-enhanced CT image shows diffusely
homogeneous enhancement. Differential diagnosis thickened loop of small bowel (arrow). Differential
includes submucosal epithelial gastric malignancy. diagnosis includes inflammatory bowel disease.
Imaging features are not specific for lymphoma in Imaging features presented are not specific for
this case. Endoscopic biopsy revealed mucosa- lymphoma. Resection of small bowel revealed diffuse
associated lymphoid tissue lymphoma. large B-cell lymphoma.
erative disorders or lymphoma. T-cell lym ever, the submucosal location of most lym
phomas are particularly prone to bowel wall phomas may cause difficulty in obtaining
involvement in the ileum and jejunum. They sufficient tissue for diagnosis.
Fig. 11—48-year-old woman who presented with are aggressive tumors with higher rates of As in esophageal lymphoma, gastric lym
vaginal discharge.
A, Contrast-enhanced CT image shows infiltrative perforation as a result [26]. phoma may have many varied appearances at
soft tissue (arrow) centered in cervix and extending As we mentioned earlier, the esophagus is imaging. Mucosal lesions are best shown at im
into parametria. Biopsy results revealed diffuse the least common site of gastrointestinal tract aging by upper gastrointestinal barium studies.
large B-cell lymphoma.
B, Contrast-enhanced CT image obtained after
involvement. Like the stomach, the esopha Diffuse nodular thickening of the gastric rugae
treatment shows good response to chemotherapy gus contains no MALT tissue, but lympho may be confused with Ménétrier disease, al
with resolution of abnormal cervical soft tissue ma may develop in the presence of Barrett though the latter has a propensity to involve the
(arrow). Primary differential consideration is cervical esophagus. The appearances of esophageal proximal half of the stomach, with lymphoma
carcinoma. Imaging features are not specific in this
case. lymphoma are difficult to differentiate from tous thickening usually seen in the antrum or
epithelial esophageal malignancies with an pylorus [24]. A submucosal lesion with central
between primary gastrointestinal tract lympho nular lesions, irregular strictures, polypoid ulceration—that is, a typical bull’s-eye appear
ma, in which there is little retroperitoneal masses, and ulcerative lesions [27]. Esopha ance—may be seen. This sign is by no means
lymphadenopathy or hepatosplenomegaly, geal biopsy is required for diagnosis; how specific, however, with a similar appearance
and involvement of the gastrointestinal tract
in disseminated NHL from other body sites.
Both the imaging features and prognosis are
distinctly different. Primary gastrointestinal
lymphoma carries a better prognosis than in
volvement in disseminated disease. The sites
of disease in order of decreasing frequency
are the stomach, small intestine, colon, and
esophagus. Primary gastrointestinal lympho
mas are usually mucosa-associated lymphoid
tissue lymphomas, also referred to as
“MALTomas,” except in the stomach, which
contains no MALT tissue. The prevalence of
gastric lymphoma can be explained as fol Fig. 14—82-year-old man who presented with anemia Fig. 15—69-year-old woman who presented with
lows: MALT tissue arises in abnormal loca and abdominal mass. Axial contrast-enhanced abdominal pain and history of diverticular disease.
tions (e.g., stomach, thyroid, ocular adnexa) in CT image shows aneurysmal dilatation of loop of Axial contrast-enhanced (oral and IV media) CT
thickened small bowel (white arrow) that has been image shows large pelvic cavitating lesion (arrow)
response to chronic antigen stimulation. In the infiltrated by disseminated non-Hodgkin lymphoma arising from ileocecal lymphomatous perforation.
case of the stomach, this stimulation is thought and left renal deposit (black arrow). Although other Resection showed diffuse large B-cell lymphoma.
to be caused by Helicobacter pylori infection differentials to consider include other inflammatory Other differential diagnoses include large pelvic
[24, 25]. Repetitive stimulation by antigens is small-bowel diseases, aneurysmal dilatation and abscess secondary to diverticular perforation.
renal deposit make lymphoma most likely diagnosis Imaging features are not specific for lymphoma in
thought to promote monoclonal cell lines that in this case. Ultrasound-guided biopsy of mesenteric this case.
are more likely to develop into lymphoprolif lesion revealed diffuse large B-cell lymphoma.
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F O R YO U R I N F O R M AT I O N
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The reader’s attention is directed to part 1 accompanying this article, titled “Extranodal Lymphoma From
Head to Toe: Part 1, The Head and Spine,” which begins on page 350.
F O R YO U R I N F O R M AT I O N
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