AJR 2000; 174:671-675
© American Roentgen Ray Society
Imaging Findings in Pancreatic Lymphoma
Differential Aspects
Elmar M. Merkle1,2,
Greg N. Bender3 and
Hans-Juergen Brambs1
1
Department of Diagnostic Radiology, University of Ulm, Robert-Koch St. 8,
89081 Ulm, Germany.
2
Department of Radiology/MRI, University Hospitals, Case Western Reserve
University, 11100 Euclid Ave., Cleveland, OH 44106.
3
Department of Radiologic Pathology, Armed Forces Institute of Pathology, 6825
16th St. N.W., Washington, DC 20306-6000.
Received June 3, 1999;
accepted after revision August 9, 1999.
Address correspondence to E. M. Merkle.
Introduction
Primary pancreatic lymphoma is a rare extranodal manifestation of any
histopathologic subtype of B-cell non-Hodgkin's lymphoma that predominantly
involves the pancreas at a disease stage of either IE or
IIE according to the modified Ann Arbor staging system. Instead of
being primary in the gland, pancreatic lymphoma can also represent direct
extension from adjacent peripancreatic lymphadenopathy. Diagnostic criteria of
primary pancreatic lymphoma include a pancreatic mass that predominates with
gross involvement of only the peripancreatic lymph nodes, no hepatic or
splenic involvement, no palpable superficial lymphadenopathy, no enlargement
of the mediastinal lymph nodes on chest radiography, and a normal leukocyte
count [1]. Although the
pancreatic gland is involved secondarily in more than 30% of patients with
non-Hodgkin's lymphoma [1],
primary manifestation is rare. Fewer than 2% of extranodal non-Hodgkin's
lymphomas arise in the pancreas
[2,
3]. The incidence increases to
5% in HIV patients because the gastrointestinal tract is the most commonly
affected extranodal site in AIDS-related non-Hodgkin's lymphoma
[4,5,6].
Imaging plays a key role in the diagnosis and staging of pancreatic masses
[7,
8]. Lymphoma certainly falls
into this group of diseases. Any radiologist imaging the pancreas must be
familiar with the imaging findings of pancreatic lymphoma because treatment
and prognosis differ significantly from those for adenocarcinoma.
Clinical Appearance
An extensive international literature review revealed a total of 85
reported patients (51 men, 34 women; age range, 23-89 years; mean age, 56
years) with biopsy-proven non-Hodgkin's lymphoma primarily involving the
pancreas
[1,2,3,
5,
9,10,11,12,13,14,15,16,17,18,19,20,21,22,23].
The duration of symptoms ranged from 2 days to 32 months, with an average of
19 weeks. The clinical findings were as follows: pain, 62 (73%) patients;
weight loss, 43 (51%) patients; jaundice, 36 (42%); nausea, 29 (34%);
vomiting, 15 (18%); fatigue, eight (9%); fever, chills, and night sweats, six
(7%); diarrhea, two (2%); gastrointestinal bleeding, two (2%); and gastric
outlet syndrome, two (2%).
The largest single study involved 12 patients
[1,
8] with most other reports
describing isolated case reports. The small number of patients per study has
lead to several conclusions that are in contradistinction to the authors'
findings. For example, the mean age of patients with pancreatic lymphoma
varied widely, yet Tuchek et al.
[3] reported a mean age of 68
years in their seven patients. They considered this finding a key differential
point when compared with patients with adenocarcinoma with a mean age of 58
years. Ezzat et al. [12]
reported the mean duration of symptoms to be 5 weeks (range, 3-8 weeks) before
medical examination and treatment in their five patients. This finding was in
direct contrast to patients with pancreatic adenocarcinoma, who present with a
mean symptom duration of 4 months. The data in the present analysis show no
significant difference regarding patient age or duration of symptoms between
patients with non-Hodgkin's lymphoma primarily involving the pancreas and
patients with pancreatic adenocarcinoma.
Although the clinical presentation of primary pancreatic lymphoma is
nonspecific, some findings may strengthen the clinical suspicion of lymphoma
rather than pancreatic cancer. The most common findings were abdominal pain
and weight loss. Although representing classic symptoms of nodal non-Hodgkin's
lymphoma, fever, chills, and night sweats were found in only 2% of patients
with primary or predominante pancreatic involvement. They certainly were not
helpful signs in this diagnosis. Fortunately, jaundice was an infrequent
finding, despite large lymphomatous masses involving the pancreatic head
[1]. In summary, only the
clinical presentation of abdominal pain and a palpable mass without jaundice
was valuable in attempting to distinguish most patients with pancreatic
adenocarcinoma from those in the minority with lymphoma. At least, such
clinical findings should suggest that a pancreatic mass might represent an
unusual neoplasm [1].
Imaging Findings
Conventional Radiography and Angiography
Untreated pancreatic lymphoma does not contain calcifications; therefore,
radiographs of the abdomen are of little value
[9,
21]. Barium examination of the
upper gastrointestinal tract may show duodenal effacement
[3], reflecting a large tumor
mass, but it is performed only in a minority of patients.
Conventional angiography shows patency of the peripancreatic vessels in
most patients (Fig.
1A,1B,1C,1D).
Encasement of the proximal superior mesenteric artery occurs in 12%
[1,
2,
9] of patients stenosis of the
superior mesenteric vein or the confluence of the portal and superior
mesenteric veins in 5% [9], and
splenic vein occlusion in 4% of all reported cases
[9]. These imaging findings
differ from those found in patients with pancreatic adenocarcinoma, in whom
vessel stenosis or occlusion is common. The vascular findings reported were
those of incremental CT studies because no conventional angiographic findings
are available for review in the current literature that address pancreatic
lymphoma.
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Fig. 1A. —70-year-old man with 3-week history of jaundice. Percutaneous
transhepatic cholangiogram shows filiform stenosis of common bile duct
(arrows). Note marked dilatation of intrahepatic bile ducts.
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Fig. 1B. —70-year-old man with 3-week history of jaundice. Transabdominal
sonogram shows hypoechoic mass (solid arrows) confined to pancreatic
head. Note lack of increased through-transmission. Dilatation of common bile
duct is also seen (dashed arrows).
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Fig. 1D. —70-year-old man with 3-week history of jaundice. Gross pathology
specimen reveals firm tan mass abutting but not invading common bile duct
(arrow). Histology (not shown) revealed B-cell non-Hodgkin's
lymphoma.
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Percutaneous and Endoscopic Sonography
On sonography, primary pancreatic lymphoma usually appears as a bulky
homogeneous hypoechoic mass confined to the pancreas without increased
through-transmission [11,
17,
19] (Fig.
1A,1B,1C,1D).
Lesion size based on the imaging and surgical data of 59 patients ranges from
3 to 21 cm, with a mean diameter of 7 cm. In the current literature, only half
the articles
[10,11,12,
17,
19,
20] provide a representative
sonogram showing the findings of pancreatic lymphoma
[11,
19,
20]. Transabdominal sonography
allows the detection of enlarged peripancreatic and periaortic lymph nodes and
dilatation of the common bile and pancreatic ducts. Recent developments, such
as Doppler waveform scanning, provide helpful information about the patency of
the major peripancreatic vessels, the celiac and superior mesenteric arteries,
and the portal, superior mesenteric, and splenic veins.
To our knowledge only a single case using endoscopic sonography in a
patient with primary pancreatic lymphoma was reported in the current
literature. Flamenbaum et al.
[14] described the typical
endoscopic sonography findings (on the basis of one case): "a strongly
hypoechogenic appearance in the pancreas, hypertrophy in all its segments, a
hyperechoic wall in the common pancreatic duct contrasting with the adjacent
parenchyma, and multiple isoechogenic peripancreatic lymph nodes." These
authors concluded that the endoscopic sonography findings were highly specific
and allowed distinction of lymphoma from all other pancreatic tumors. This
conclusion was based on one case, and although the conclusions are logical, a
larger sample size is needed for confirmation.
CT
CT is by far the most common imaging technique used in the detection and
characterization of primary pancreatic lymphoma. Most lesions are less dense
than muscle and appear homogeneous
[21] (Figs.
2A,2B,3A,3B,3C,4A,4B,4C,4D,4E,4F).
Small heterogeneous areas within a tumor mass can be seen in isolated cases
[2,
9], and, therefore, do not
allow exclusion of the diagnosis of primary pancreatic lymphoma (Fig.
5A,5B,5C,5D,5E).
Enhancement after administration of IV contrast medium is usually poor yet
homogeneous [21].
Heterogeneous enhancement was reported in isolated cases
[9], but this finding alone
prevents differentiation from adenocarcinoma. On CT, two different morphologic
patterns of pancreatic involvement are seen: a localized, well-circumscribed
tumoral form and diffuse enlargement infiltrating or replacing most of the
pancreatic gland [9] (Figs.
2A,2B,3A,3B,3C,4A,4B,4C,4D,4E,4F,5A,5B,5C,5D,5E).
The diffuse infiltrating pattern may mimic the imaging findings of acute
pancreatitis with gland enlargement and irregular infiltration of the
peripancreatic fat [9].
Patients with this pattern, however, never show the typical clinical signs of
acute pancreatitis even if the serum amylase level is elevated
[1,
3,
11,
20]. The well-circumscribed
tumoral form can be easily misinterpreted as a ductal adenocarcinoma,
especially in patients with dilatation or encasement of the pancreatic and
common bile ducts. Dilatation of Wirsung's duct is usually mild, with a ratio
of duct diameter to distal gland width invariably less than 0.5
[9]. This combination of a
bulky localized tumor in the pancreatic head without significant dilatation of
the main pancreatic duct strengthens a diagnosis of pancreatic lymphoma over
adenocarcinoma. Furthermore, if enlarged lymph nodes are encountered below the
level of the renal veins, virtual exclusion of adenocarcinoma is possible
[21].
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Fig. 2B. —51-year-old man with 2-month history of jaundice. ERCP Shows
filiform stenosis of common bile duct (solid arrows). Note normal
caliber of Wirsung's duct (dashed arrows). At surgery, tumor proved
to be non-Hodgkin's lymphoma. Needle biopsy of left kidney revealed focal
chronic interstitial nephritis.
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Fig. 3A. —5-year-old girl with 3-week history of abdominal pain, intermittent
nausea and vomiting, and jaundice. Unenhanced CT scan shows diffuse
enlargement of pancreatic head (white arrows) with marked dilatation
of intrahepatic bile ducts (black arrows).
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Fig. 3B. —5-year-old girl with 3-week history of abdominal pain, intermittent
nausea and vomiting, and jaundice. CT scan after contrast medium
administration shows tumor having only mild enhancement but better
demarcated.
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Fig. 3C. —5-year-old girl with 3-week history of abdominal pain, intermittent
nausea and vomiting, and jaundice. Gross pathology specimen reveals firm tan
mass abutting but not invading duodenum. Note only mild dilatation of
Wirsung's duct despite huge tumorous mass in pancreatic head. Histology
revealed intermediate grade, B-cell non-Hodgkin's lymphoma.
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Fig. 4A. —67-year-old man with history of painless jaundice. Unenhanced
helical CT scan shows circumscribed enlargement of pancreatic head
(arrowheads). Solid arrow marks endoscopically placed biliary stent.
Note gallstone (dashed arrow).
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Fig. 4D. —67-year-old man with history of painless jaundice. Contrast-enhanced
T1-weighted MR image with fat saturation shows inhomogeneous enhancement with
hypointense areas (solid arrows) within enlarged pancreatic head.
Note stent in common bile duct (dashed arrow).
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Fig. 4F. —67-year-old man with history of painless jaundice. T2-weighted
out-of-phase MR image shows tumor but also points out patency of superior
mesenteric artery, inferior caval vein, and portal vein (arrows) and
slight dilatation of Wirsung's duct (arrowheads). At surgery, tumor
was shown to be high-grade centroblastic non-hodgkin's lymphoma.
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Fig. 5A. —60-year-old woman with 1-month history of abdominal pain.
Contrast-enhanced helical CT scan shows diffuse enlargement of pancreas with
hypodense areas (arrows) and encasement of splenic vessels. Note
enlarged retrocaval lymph node (arrowheads).
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Fig. 5D. —60-year-old woman with 1-month history of abdominal pain.
Contrast-enhanced T1-weighted MR image shows inhomogeneous enhancement with
hypointense areas (arrows) within enlarged pancreas.
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Fig. 5E. —60-year-old woman with 1-month history of abdominal pain. Enlarged
lymph nodes (arrows) are also encountered on contrast-enhanced
T1-weighted MR image below level of renal veins. Percutaneous sonographically
guided pancreatic tail biopsy revealed high-grade centroblastic non-Hodgkin's
lymphoma.
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Prayer et al. [21]
described invasive tumor growth not respecting anatomic boundaries and
infiltrating retroperitoneal or upper abdominal organs and the
gastrointestinal tract as an additional reliable sign for non-Hodgkin's
lymphoma. This conclusion was supported by Van Beers et al.
[9], who also reported adjacent
duodenal invasion in three of eight patients. Neither calcification nor
necrosis within the tumor mass was described in any case of untreated
pancreatic lymphoma. Presence of calcification or necrosis are reliable
findings for ruling out non-Hodgkin's lymphoma
[21].
Performing a contrast-enhanced scan with current helical CT arterial phase
techniques reliably assesses patency of the main pancreatic vessels and
adjacent arteries and veins. Imaging findings show encasement of the superior
mesenteric artery and stenosis or occlusion of the superior mesenteric,
splenic, or portal vein in a minority of cases
[9].
ERCP and Percutaneous Transhepatic Choledochography
The findings of 10 ERCPs of Wirsung's duct appearance were reported in
detail in the current literature. Thirty percent showed a normal duct
appearance, 10% ductal displacement, 50% mild duct stenosis, and 10% stricture
of the main pancreatic duct. Severe distal dilatation of Wirsung's duct was
not reported [3,
10,
17,18,19,20]
(Figs.
2A,2B,3A,3B,3C).
Seven other cases in which CT was used suggested only mild dilatation of
Wirsung's duct [2,
9]. Thus, unlike pancreatic
adenocarcinoma, moderate to severe dilatation of Wirsung's duct is apparently
rare in pancreatic lymphoma because Wirsung's duct is either normal,
displaced, or simply narrowed in patients with pancreatic lymphoma.
Bile duct dilatation from obstruction is seen more often (Figs.
1A,1B,1C,1D,2A,2B,3A,3B,3C)
because jaundice occurs in 42% of patients with non-Hodgkin's lymphoma
primarily involving the pancreas. Usually, endoscopic or percutaneous stent
insertion is performed as a preliminary treatment procedure (Fig.
4A,4B,4C,4D,4E,4F).
MR Imaging
To our knowledge, MR imaging findings in patients with primary pancreatic
lymphoma are not reported in the literature. We observed two different
morphologic patterns of pancreatic involvement seen on MR imaging that are
similar to the CT appearance. The well-circumscribed tumoral type (Fig.
4A,4B,4C,4D,4E,4F)
appears as a low-signal-intensity homogeneous mass within the pancreas on
T1-weighted images with subtle enhancement after IV administration of
gadolinium-containing contrast medium. On T2-weighted images, a tumoral mass
shows a more heterogeneous character with a low to intermediate signal
amplitude slightly higher than that of the residual gland but much lower than
the signal intensity of fluid. The diffuse infiltrating type of pancreatic
involvement shows similar characteristics of low signal intensity on
unenhanced T1- and T2-weighted images, with mild to moderate enhancement after
gadolinium injection. In the diffuse infiltrating type, enhancement is
predominately homogeneous but may include small foci of little or no
gadolinium uptake (Fig.
5A,5B,5C,5D,5E).
In general, bile and pancreatic ductal dilatation can be easily assessed with
MR imaging using MR cholangiopancreatography
[24]. Only mild pancreatic
ductal dilatation is visible on the MR imaging cases presented. Furthermore,
MR imaging is equivalent to CT regarding information about the peripancreatic
vessels and enlarged lymph nodes. Additional information is obtained when MR
angiography is used [24].
Definitive Diagnosis, Treatment, and Prognosis
Percutaneous or endoscopic core biopsy should be performed to establish the
diagnosis. In early reports, because percutaneous imagingguided biopsy was not
considered an accurate diagnostic tool, the correct diagnosis was rarely made
[3,
18,
22]. This attitude has changed
significantly in the last decade. From 38 percutaneous or endoscopic biopsies
of pancreatic lymphoma reported in recent literature
[1,
3,
9,
12,13,14,
16,
21,22,23,
25,
26], 25 cases (66%) were
correctly diagnosed. In an additional two patients (5%), the specimen was
suggestive but not diagnostic of lymphoma. In most patients, the diagnosis can
be established without surgery; this fact is a major reason to look for
findings suggestive of pancreatic lymphoma.
Chemotherapy is the treatment of choice for most patients with pancreatic
lymphoma. The most common regimen includes cyclophosphamide, doxorubicin
hydrochloride, vincristine, and prednisone. Adjuvant surgery discussed in the
literature is controversial. Some surgeons advocate a choledochojejunostomy in
patients with jaundice as a fast and permanent treatment option
[1,
10]. Other groups perform
transient endoscopic or percutaneous stenting for biliary drainage
[16,
23]. Only technical
information about pancreatic stenting is provided in the current literature.
Surgical tumor debulking is not generally accepted and is suggested in only
one report [1]. The role of
radiation therapy is also not yet defined except as an adjuvant to
chemotherapy. Using complex treatment approaches, cure rates of up to 30% are
reported for patients with primary pancreatic lymphoma
[10]. This prognosis is much
better than the dismal 5% 5-year survival rate in patients with pancreatic
adenocarcinoma.
Summary
When the radiologist is faced with a well-circumscribed tumoral mass in the
pancreas, knowing when to direct the patient toward non-surgical biopsy
instead of surgical biopsy and staging is critical. Lymphoma does not require
surgical staging or a palliative Whipple's procedure before chemotherapy or
radiation therapy. A better overall prognosis with nonsurgical treatment is
additional impetus to search for secondary signs of primary pancreatic
lymphoma. In patients with primary pancreatic lymphoma, no marked pancreatic
ductal dilatation is present even with ductal invasion. Adenocarcinoma
commonly dilates the more distal pancreatic duct when more proximal ductal
invasion has taken place. Lymph node involvement below the level of the renal
veins was another finding not seen with adenocarcinoma. Clinical and imaging
findings are otherwise not specific in the differentiation of pancreatic
lymphoma and pancreatic cancer, but a bulky homogeneous tumoral mass without
alteration of Wirsung's duct or the peripancreatic vessels should suggest the
diagnosis. In patients with diffuse infiltration of the pancreatic gland
without clinical signs of pancreatitis, the radiologist should be alert to the
possibility of pancreatic lymphoma.
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Introduction
Clinical Appearance
