Non-Hodgkin Lymphoma of the Small Intestine1 Stephen E. Rubesin, MD #{149} Alison M. Gilc/,rist, MD2 Mary Bronner, MD #{149} Scott H. Saul, MD3 Hans Herlinger, MD #{149}Kathryn Grumbach, MD #{149} Marc S. Levine, MD #{149}Igor Laufer, MD
The
authors
Hodgkin system cases
present
a simplified
radiographic
lymphoma involving is based on radiographic of
lymphoma
the small findings
involving
the
small
classification of nonintestine. The classification in 22 pathologically proved
bowel
and
consists
of
three
major forms: primary, lymphoma complicating celiac disease, and mesenteric nodal. In this series, small bowel lymphoma was evenly distributed in the jejunum and ileum. The most common radiographic patterns were circumferential lesion (seven cases) cavitary lesion (four cases) and mesenteric nodal disease invading the small bowel (seven cases) Obstructive symptoms were usually encountered with the mesenteric nodal form. Lymphoma complicating celiac disease was typified by multiple, thickened, nodular folds involving a segment of proximal small intestine. ,
,
.
U INTRODUCTION Small bowel lymphoma either by gastrointestinal 20% of primary
is defined symptoms
tract tumor that is manifested mass (1 -3) Approximately tumors in the small bowel are lymphoma (4,5). Almost are non-Hodgkin lymphoma (6) Most of these tumors a diffuse histologic pattern, and are composed of large
malignant
all small bowel lymphomas are of B cell origin, have lymphoid cells. In this article, we correlate Hodgkin lymphoma involving
as an alimentary or an abdominal
.
.
the radiologic and pathologic the small bowel. We present
manifestations a simplified
of nonclassifica-
tion system for non-Hodgkin lymphoma involving the small bowel, in which the disease is classified into three major forms: a primary form, lymphoma complicating celiac disease, and a mesenteric nodal form. Each of these forms has distinct radiographic patterns. Recognition of the type of bowel involvement may direct further workup of the patient or help in treatment planning. Abbreviation: Index
H-E
terms:
Intestinal
RadioGraphics I
From
the
1990;
the
hematoxylin-eosin
Departments
University
neoplasms,
March
quests
to S.E.R.
27,
2 Current
address:
Current ‘C RSNA,
address: 1990
1990; X-Ray
#{149} Intestinal
neoplasms,
staging,
74.34
Lymphoma,
staging,
#{149}
74.34
10:985-998 ofRadiology
of Pennsylvania,
ceived
74.34
revision
Spruce
requested
Department,
Department
(S.E.R.,
3400
Stirling
of Pathology,
A.M.G.,
H.H.,
KG.,
St, Philadelphia, April Royal Chester
18 and
M.S.L.,
PA I 9 1 04 received
Infirmary, County
IL.) .
and
From
the
Pathology 1 989
May 9; acceptedJune Livilands,
Hospital,
Stirling, West
Chester,
(MB., RSNA 14.
S.H.S.),
scientific
Address
Hospital assembly.
reprint
of’ Re-
re-
Scotland. Penn.
985
Table 1 Clinical Summary
of Patients
with
Non-Hodgkin
Lymphoma
ing
Involv
the
Sm all Bowel
Symptoms Form of Involvement
Abdommat Pain
Signs
Average Age (y)
Primary Comp!icating celiacdisease Mesenteric nodal
11
63
6
2
3
2
4
61
1
0
0
0
7
43
3
0
5
5
5
All
22
56
10
2
8
7
6t
A
t
See discussion of individual Excludes data from patients
Fever
Nausea
cases in text and in figure with celiac disease.
Table 2 Number
and
follow-through enema (CT)
0
0 7
4 8
Size
of Lesions No. of Patients
Average Length (cm)
Range (cm) 4-30 4-13
Total
22
12
4-30
enced
with symptoms
,
tions, 1 1 small bowel computed tomographic
4
13 8
of small bowel disease. The disease was confirmed with exploratory laparotomy in 20 patients (with bowel resection in 1 9) endoscopic biopsy and autopsy in one, and autopsy alone in one. Fif-
teen small bowel
4
19 3
We based our classification system on data from 22 adults with pathologically proved non-Hodgkin lymphoma involving the jejunum and ileum, who presented at the Hospital of the University of Pennsylvania and the Philadelphia Veterans Administration Hospi. tal from 1977 to 1989. We included only those patients for whom adequate radiologic studies and surgical or autopsy proof were available. We excluded (a) all patients with disseminated lymphoma (involving the spleen, liver, small bowel, and lymph nodes) at the time of initial diagnosis and (b) all patients who had a history of nodal lymphoma
presented
*
3
Solitary Multifocal
POPULATION
who subsequently
7
legends.
Type of Involvement
U CLINICAL
Vomiting
Abdomma! Mass
Weight Loss
Duration (mo)
No. of Patients
examinastudies, and studies were
13
reviewed.
tients.
by approximately one-third of the paPyrexia was seen in only two patients.
S Predisposing Conditions Non-Hodgkin lymphoma of the small bowel has been associated with acquired immunodeficiency syndrome (AIDS), celiac disease, systemic lupus erythematosus, Crohn dis-
ease, and chemotherapy
undergone
radiation
(7,8) Two systemic
of our lupus
.
patients had long-standing erythematosus. One patient tory of mediastinal Hodgkin
had a 6-year hisdisease
therapy,
and
had
chemotherapy,
and autologous bone marrow transplantaiion. No patients with AIDS or Mediterranean lymphoma were seen in our series.
. RADIOGRAPHIC FINDINGS Lymphoma involving the small intestine tends to involve longer segments of bowel comparison with primary adenocarcinoma. In our series, the average length of diseased bowel was 1 2 cm. Although small bowel non-Hodgkin
lymphoma
is usually
in
a solitary
lesion,
multiple sites are involved in 10%25% of cases (6) In our series, three of 22 patients had multiple lesions (Table 2). In children and young adults, lymphoma primarily affects the ileocecal region (5,6). In adults, most investigators have found that .
.
Symptoms
and
Signs
All patients presented with symptoms related to the small bowel. Abdominal pain was the most frequent symptom, experienced by about half the patients (Table 1) Nausea, vomiting, and weight loss were also experi.
986
#{149}Ra4ioGrapbks
#{149} Rubesin
et al
the ileum, especially the distal ileum, the most frequent site of tumor (6,9)
Volume
10
was .
In our
Number
6
Table
3 of Non-Hodgkin
Distribution Bowel Form
Lymphoma
Proximal
Primary Complicating celiac disease Mesenteric nodal All Note
in the Small
-Numbers
represent
Middle
Distal
5
3
3
3 1
1 5
0 1
9
9
4
number
of patients.
I
Figure 1. Circumferential lymphoma. A 79-year-old woman with a right upper quadrant mass underwent a small bowel followthrough examination. Spot radiograph from that examination shows a 1 2-cm-long lesion with a mildly increased luminal diameter, irregular contour, and nodular surface pattern (arrow) At surgery, a lymphoma of the ileum was found focally invading the small bowel mesentery. Diagnosis: diffuse, large cell lymphoma. .
masses and sprue pattern. However, on the basis of our experience, we have modified this traditional classification into three categories: (a) primary form, (b) lymphoma complicating celiac disease, and (C) mesen-
teric
nodal
form.
. Primary Form Eleven of our patients had the primary form of small bowel lymphoma. In this pattern, the bulk of the lymphomatous tumor lies within
the
intestinal
direct extension tery and spread
wall,
but
into the small to the regional
often
bowel lymph
Tumor
however,
primary
phoma was evenly the small intestine with celiac disease, volved
the
proximal
small
distributed (Table 3) lymphoma jejunum
bowel .
lym-
throughout In patients usually in(Table
3).
The traditional radiographic classification of small bowel lymphoma (1 0, 1 1) has five categories: (a) multiple nodular defects, (b) infiltrating form, (C) polypoid form, (d) endoexoenteric
formation, mesenteric
November
form
with
cavitation
and
is
mesennodes.
spread to the liver, spleen, bone and distant lymph nodes may occur er. The two major radiographic patterns
marlatare a
circumferential
and a
row, series,
there
cavitary
lesion
lesion (four
(seven
patients)
patients).
Circumferential Lesion-This pattern is characterized by a sharply circumscribed annular tumor involving a relatively long segment of small bowel (Fig 1). Submucosal infiltration by tumor causes effacement of mu-
fistula
and (e) predominantly invasive form with large extraluminal
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et al
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Figure 2. Circumferential lymphoma. A 79-year-old man had a 2-year history of abdominal pain suggestive of ischemia. (a) Spot radiograph from the single-contrast phase of a small bowel enema examination shows an abrupt, annular lesion 6 cm in length with effaced mucosal folds (arrow) (Reprinted, with per. mission, from reference 8.) (b) Surgical specimen shows a sharply circumscribed lesion (arrow) with an ulcerated mucosal surface and extension into the mesentery. (c) CT scan reveals a small bowel loop with a thickened wall (arrow) (d) Low-power photomicrograph (hematoxylin-eosin [H-EJ stain) of a specimen slice. At the margin of the specimen, submucosal tumor (T) has a sharp margin and extends into the muscularis propria (arrow). Diagnosis: diffuse, large cell lymphoma. .
.
988
#{149}RadioGrapbics
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Rubesin
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a.
b. Figure 3. Circumferential lymphoma with mild dilatation. A 70-year-old man had abdominal pain, anemia, and heme-positive stool. (a) Spot radiograph from a small bowel follow-through examination shows a 14-cm-long annular lesion (arrows) with complete effacement of mucosal folds and mild lu-
minal
dilatation.
(b) CT scan demonstrates
a well-
circumscribed lesion with a markedly thickened (arrows) . (c) Surgical specimen shows a well-circumscribed, bulky tumor with a thickened wall rows) . At surgery, tumor invasion of the bladder
sigmoid ic nodal large from
mesentery
involvement cell lymphoma. reference 8.)
was found, was seen. (Reprinted,
but no local
wall (arand
mesenter-
Diagnosis: diffuse, with permission,
c.
cosal folds (Fig 1) may tact mucosa tumor. The narrowed, dilatation) mon because
November
(Fig 2) (1 2) Mucosal nodularity reflect mucosal ulceration or inoverlying nodular submucosal luminal diameter may be slightly normal, or widened (aneurysmal (Fig 3). Obstruction is uncomthe infiltrating tumor weakens .
1990
the muscularis propria of the bowel wall and does not elicit a desmoplastic response. Only one of seven patients with this pattern had clinical and radiographic signs of obstruction.
Rubesin
et al
#{149}RadioGrapbics
#{149}989
-.
a.
ITT
b.
Figure 4. Cavitary lymphoma. A 22-year-old woman with an 8-year history of systemic lupus erythematosus presented with abdominal pain and fever attributed to small bowel ischemia. (a) Spot radiograph from a small bowel followthrough examination shows a small ulcer (arrow) on the mesenteric border associated with slightly thickened folds. This lesion was not described on the initial radiographic report. (b) Eleven weeks later, the patient presented with severe abdominal pain,
tenderness,
and
fever.
Spot
radiograph
from
a small bowel enema study shows a large ulcer (short arrows) irregular nodules (curved arrow), and thickened folds (long arrows) (c) At surgery, a small intestinal tumor was found that had focal,
.
ly perforated
into
into a mesenteric
mesenteric
lymph
fat and
node.
Surgical
had spread
specimen
shows a cavity (C ). Diagnosis: diffuse, large cell lymphoma. (Fig 4a and 4c reprinted, with permission,
from
reference
8.)
C-
Cavitary Lesion.-Cavitary lesions second most frequent radiographic of primary small bowel non-Hodgkin phoma. Ulceration initially extends intramural portion of the tumor (Fig advanced lesions extending into the
are the pattern lyminto the 4) In mesen.
tei-y, ulceration may result in cavitation of the bulk of the tumor. If the cavitated mesenteric portion of the tumor perforates into the mesentery, adherence of small bowel loops and intraloop abscess formation may occur (Fig 5) Fever is an uncommon clinical finding in non-Hodgkin lymphoma involving the small bowel. In our series, the two patients with fever had cavitary lesions and confined perforations. .
990
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Rubesin
et al
Volume
10
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Figure 5. Cavitary lymphoma with focal perforation and intraloop abscess formation. A 74-yearold woman had a 5-month history of abdominal pain and weight loss and an abdominal mass. (a) Spot radiograph from a small bowel enema study shows a large, barium-filled cavity (C) along the mesenteric border of several bowel loops. (b) CT scan reveals contrast material (C) filling the lumen of a thin-walled cavitary mass (arrows) (c) Gross specimen of a 1 6-cm mass found at surgery. The mass consists of a small bowel lymphoma, which had extended into the mesentery, cavitated, and perforated, forming a mesenteric abscess (A ) surrounded by adherent .
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small
bowel
nodes
were
surgical
from v
‘
November
specimen
shows
an ulcer
surface
extending
Low-power
(Fig
5a and
from reference
1990
of 1 9 mesenteric
by lymphoma.
photomicrograph
lymph
(d) Opened (U) viewed into the cavi(H-E)
shows
tumor (T) extending from mucosal surface to the lumen of the cavity (C ). Diagnosis: diffuse, large cell lymphoma with T cell surface antigen markers.
e.
Three
the luminal
ty. (e) -
1oops.
infiltrated
Sc reprinted,
with
permission,
8.)
Rubesin
et al
U
Ra4ioGrapbics
U
991
Figures
6, 7. (6) Lymphoma complicating celiac disease. A 69-year-old woman with long. standing celiac disease presented with recurrent symptoms despite dietary restriction. Spot radiograph from a small bowel enema study shows thick, nodular
folds
(arrows)
in a 1 5-cm
loop
:‘ .
.. ,f’,
-.
of jeju,
num.
Diagnosis:
diffuse,
large
cell
#{149}1’
lymphoma.
(7) Subtle lymphoma complicating celiac disease. A 53-year.old man complained of acutely increasing diarrhea and weight loss; 6 months previously, celiac disease had been diagnosed at jejunal biopsy.
(a)
Spot
radiograph
from
a small
bowel
en-
ema study shows subtle nodular folds (arrows) the jejunum. (b) Medium-power photomicrograph (H-E) of endoscopic biopsy specimen shows villous atrophy (arrowheads) ma infiltrating the lamina propria cosa (S ) . Diagnosis: diffuse, large
with
T cell
surface
antigen
in .n’
and lympho) and submucell lymphoma
(L
markers. ..-..c.
S Lymphoma Celiac Disease
Complicating
.
,
.
U
RadioGrapbics
U
Rubesin
et al
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‘.
S
‘
S
Four patients in our series had lymphoma complicating celiac disease. Although it is a form of primary small bowel non-Hodgkin lymphoma, lymphoma complicating celiac disease is characterized by a different clinical history, location, and radiographic appearance Whereas most cases of small bowel non-Hodgkin lymphoma are of B cell origin (9) most, if not all, cases of lymphoma complicating celiac disease are of T cell origin (1 3) Patients with the latter disease usually have a long history of celiac disease and sub-
992
,.-,
%
S
-
‘
_4
,
.5’
‘1
7b.
sequently develop diarrhea, malabsorption, and weight loss despite continued dietary restriction (1 4) In some patients, initial diagnosis of celiac disease and coexistent lymphoma may be made at an elderly age. Two of our four patients had a 6-month history of severe malabsorption, weight loss, diarrhea, and no previous history of celiac disease. .
Volume
10
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Figures
8, 9.
(8) Mesenteric nodal lymphoma invadAn abdominal mass was palpated in a 55-year-old man. Spot radiograph from a small bowel enema study shows extrinsic mass impression, primarily on the mesenteric border of small bowel (large arrow); narrowing of the lumen (small arrows) ; and dilatation of proximal small bowel, a finding indicative of obstruction. At surgery, a diffuse, large cell lymphoma of the mesentery was found encasing the small intestine. (9) Mesenteric nodal lymphoma. A 52-year-old woman presented with crampy abdominal pain and vomiting. ( a) Overhead radiograph from a small bowel enema study shows separation of small bowel loops; abrupt angulation of loops (large arrow) ; tethering of folds (small arrows) ; and dilatation of proximal versus distal small
ing small bowel.
bowel, a finding indicative of (b) CT scan shows a mesenteric the mesenteric border of small rows) and focal circumferential around
fuse,
a small
large
cell
bowel
loop
partial
obstruction.
mass (m ) compressing bowel loops (small arextension of tumor
(large arrow).
Diagnosis:
dif-
lymphoma.
8.
9a.
9b.
Non-Hodgkin lymphoma in celiac disease usually involves the proximal small intestine, which is the site of the greatest villous damage and inflammation. Enlarged, nodular folds involve a variable length of small intes-
tine (Fig 6). The radiographic phoma complicating subtle,
ema
even
manifestations celiac disease
on images
from small bowel en7) (1 5) Radiographof lymphoma from ulcer-
examinations
(Fig
Ic differentiation
.
aiive jejunoileitis complicating ease may be impossible (15). .
Mesenteric
In most
teric
series,
lymph
Nodal lymphoma
nodes,
with
1990
celiac
dis-
Form arising
direct
into the small bowel, is classified bowel lymphoma (6). However,
November
of lymmay be
in mesen-
extension
that mesenteric nodal lymphoma with direct invasion of the small bowel is a distinct radiographic entity. The seven patients in our series with this form of lymphoma underwent exploratory laparotomy, five for obstructive symptoms and two for an abdominal mass. In each patient, large mesenteric masses abutted, displaced, and focally invaded the small bowel.
In six of the seven patients, no other tumor was seen. One patient had focal, retroperitoneal lymphadenopathy. The radiographic findings of mesenteric nodal lymphoma consist of mass effect along the mesenteric border of the small intestine (Fig 8) angulation of small intestinal loops (Fig 9) spiculation and tethering of the lu,
,
as small we believe
Rubesin
et al
U
Ra4ioGrapbics
U
993
a.
b.
d.
C-
Figure 10. Mesenteric nodal lymphoma. A 32-year-old woman had a left upper quadrant mass detected at routine physical examination conducted S months after cesarean section. (a) Overhead radiograph from a small bowel follow-through examination shows separation of proximal jejunal loops and extrinsic mass effect along the mesenteric border of small bowel (open arrows) and stomach (solid arrow) Focal thick.
ening
of jejunal
folds
(curved mass (M
arrows)
is seen
at the
site
of bowel
wall
invasion.
(b)
CT scan
demonstrates
a large mesenteric ) (c) Low-power photomicrograph (H-E) of specimen obtained where tumor either abutted or was adjacent to small bowel shows lymphoma (L ) extrinsic to the muscularis propria (M ) of the bowel. (d) Medium-power photomicrograph (H-E) of specimen from the site of thickened folds shows lymphoma (arrow) focally invading through the muscularis propria (M ) into the submucosa (S
994
U
RadioGraphics
) Diagnosis:
diffuse,
.
U
Rubesin
.
large
cell
et al
lymphoma.
Volume
10
Number
6
“3
M
Figure 11. Mesenteric nodal lymphoma. A 23year-old man had a 6-year history of mediastinal Hodgkin disease treated with radiation therapy, chemotherapy, and autologous bone marrow
:;.i
transplantation. He had a stable (a) Spot radiograph from small
r
A
mediastinal mass. bowel follow-
through examination shows a smooth, extrinsic mass impression on the mesenteric border (arrows) of a loop of the midportion of the small
bowel.
(b)
Four months
later,
the patient
com-
plained of vomiting. Spot radiograph from small bowel follow-through examination shows enlargement of the mesenteric mass, with spiculalion and tethering (arrows) of the mesenteric bor-
der of the small C-
minal small folds
contour, and variable narrowing of the intestinal lumen. Thickened nodular in the region of tethering indicate areas
of tumor invasion of the small bowel (Fig 1 0) In one patient, radiologic studies showed clear progression from an extrinsic
bowel,
and narrowing
of small
bowel loops. Dilatation of the proximal small bowel was seen. (C) CT scan obtained at the same time as b shows a large mesenteric mass (M ) . At surgery, there was partial small bowel obstruction and a mesenteric mass focally invading the serosa of the small bowel. Diagnosis: diffuse, large cell lymphoma with histologic characteristics distinct from those of Hodgkin disease.
.
mesenteric
mass
tine to a mesenteric structing the small
November
1990
compressing
mass bowel
the
small
intes-
invading and ob(Fig 11).
Rubesin
et al
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Figure
12.
Target
lesions.
A 55-year-old
woman
with
a 3-year
history
of lymphoma
involving
axillary
and
ingumnal lymph nodes complained of abdominal pain. (a) Spot radiograph demonstrates two sharply circumscribed lesions with smooth surfaces and central ulceration (arrows) along the greater curvature of the stomach. (b) Another spot radiograph shows numerous target lesions (arrows) in the duodenum. p = papilla of Vater. (c) Spot radiograph from small bowel follow-through examination shows a target lesion (arrow) in the jejunum. (d) At surgery, numerous nodules were found in the jejunum. Medium-power photomicrograph (H-E) of the pathologic specimen shows submucosal tumor (T) below the muscularis mucosae (arrow) Tumor focally invades the mucosa (M ) and underlies a large mucosal ulcer (U) DiagflO5iS: disseminated large cell lymphoma. (The patient was not included in our series because of the disseminated nature of her disease.)
.
.
Unusual
.
Radiographic
Patterns
Target Lesions.-Submucosal masses with central ulceration (target lesions) are an Uncommon appearance of non-Hodgkin lymphoma involving the small intestine. We have seen only one case of lymphomatous target
the
lesions
case
in the
was
not
small
included
bowel.
in this
However,
series
be-
cause the non-Hodgkin
U
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U
Rubesin
et al
nodal
SmallNodules.-Although mu!nodules involving long segments of the bowel have been reported as a comradiographic manifestation of non-
Numerous
tiple small mon Hodgkin
countered
996
patient had disseminated lymphoma (Fig 12).
lymphoma
this
pattern
(1 6),
we
during
Volume
have
the
10
not
past
en-
12
Number
6
13.
Figures
13, 14.
lar pattern.
(13)
graph
from
small
study
shows
3-5
Diffuse Spot
bowel
numerous
mm in diameter
small
bowel
loops.
nodu-
radio-
enema nodules
carpeting Nodules
are
more conspicuous than thickened folds. (Courtesy of Dean D. T. Maglinte, MD, Methodist Hospital, Indianapolis.) (14) Alpha chain disease (Mediterranean lymphoma) Overhead radiograph shows numerous small nodules (arrow) distorting the entire surface of the small intestine. No narrowing is seen. (Courtesy of Emeric Lax, MD, Hadassah University Hospital, Jerusalem; reprinted, with permission, from reference 1.)
.
.;:v’
14.
patients were not included cause they were from other
two These in our series beinstitutions. We
are uncertain
nodular
years.
For
examples
represents volving
November
completeness,
we
of this pattern
(Figs
if the diffuse (a)
multiple
illustrate
13
,
1 4)
pattern
disseminated lymphoma organ systems, lymph
1990
.
nodes, and small bowel; (b) lymphoma associated with immunodeficiency states; or (c) Mediterranean lymphoma. Patients with Mediterranean lymphoma (alpha chain disease, immunoproliferative
in-
Rubesin
et al
U
Ra4ioGrapbics
U
997
small
intestinal
disease)
present
with
.
tered
any patients
with
this disease
REFERENCES
U
diar-
rhea and malabsorption. The plasma cells involving the immunoglobulin-secreting system produce immunoglobulin molecules with incomplete alpha chains, devoid of light chains. A lymphomatous proliferation is seen in the lamina propria and submucosa of long segments of small bowel, which is demonstrated radiographically as diffuse mucosal nodularity (Fig 1 4) Mesenteric lymph nodes and liver may be infiltrated by tumor. Alpha chain disease is extremely rare in Western countries, and we have not encoun-
at our in-
.
1
41. Rachmilewitz
2.
3
.
Although ries
authors
state
quent ing
that
site the
these
distal
many ileum
of non-Hodgkin
small
bowel,
tumors
jejunum
reporting
the
were
and
4
.
in our
series
se-
most
lymphoma
evenly
ileum.
other
is the
fre-
of adults,
Non-Hodgkin
ease,
and the mesenteric
nodal
form.
tation
occurring
predominantly
of proximal
small
intestine
with
ened
nodular
folds
in the center
of the
process are suggestive of invasion of the muscularis propria or submucosa. The mesenteric nodal form is the type of lymphoma that usually is accompanied by obstruction. Another type-numerous small nodules diffusely involving long segments of the small intestine-is
rare
and
nated nodal lymphoma, phoma, or other primary
may
be
1978;
8.
9.
due
Mediterranean lymphoma.
MP, Walsh
involve-
150 cases.
Cancer
1985;
55:1060-
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879. 1 0.
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Marshak RH, Lindner AE. Radiology of the small intestine. 2nd ed. Philadelphia: Saunders, 1976. Marshak RH, Lindner AE, Maklansky D. Lymphoreticular disorders of the gastromntestinal tract : roentgenographic features. Gastrointest Radiol 1979; 4:103-120.
1 2.
Levine
thickened
nodular folds. The mesenteric nodal form appears as an extrinsic mass along the mesenteric border of the small bowel, with angulaiion of loops and tethering of folds. Thick-
Gastrointestinal
Brady LW, Asbell SO. Malignant lymphoma of the gastrointestinal tract. Radiology 1980; 137:291-298. Gilchrist AM, Herlinger H, Carr RF, Saul SH, Levine MS. Small bowel lymphoma: a radiologic/pathologic correlation . Gastrointest
the
complicating as a segment
1985; 1965-1973. R, Panahon AM, Barcos
L.
in-
7.
The pri-
along
mesenteric border. Lymphoma celiac disease usually appears
small
Lewin KJ, Ranchod M, Dorfman phomas of the gastrointestinal
lymphoma
mary form appears either as a circumferential lesion with effaced mucosal folds and varying luminal width or as an ulcer or cavi-
Primary
6.
in the
associated with celiac disease usually involved the proximal small intestine. We have presented a simplified version of the traditional radiographic classification of primary non-Hodgkin lymphoma involving the small intestine. Three major forms are seen in Western populations: the primary form, lymphoma complicating celiac dis-
E.
In: BerkJE, ed. Bockus 4th ed. Philadelphia:
ment in non-Hodgkin’s lymphoma. Cancer 1980; 46:215-222. Craig 0, Gregson R. Primary lymphoma of the gastrointestinal tract. Clin Radio! 1981; 32:63-71. Dragosics B, Bauer P, Radaszkiewicz T. Primary gastrointestinal non-Hodgkin’s lymphomas: a retrospective clmnicopathologic
studyof 1073.
involv-
distributed
Saunders, Herrmann
D, Sturzman
S.
SUMMARY
D, Okon
testinal lymphoma. gastroenterology.
stitution. U
Herlinger H, Maglinte DDT. Tumors of the small intestine. In: Herlinger H, Maglinte D, eds. Clinical radiology of the small intestine. Philadelphia: Saunders, 1989; 299-
MS, Drooz
malignancies testRadiol
AT, Herlinger
of the small bowel. 1987; 12:53-58.
PG, SpencerJ,
Connolly
H.
Annular
Gastroin-
1 3.
Isaacson
14.
Malignant histiocytosis of the intestine: cell lymphoma. Lancet 1985; 2:688-691. Swinson CM, Slavin G, Coles EC, Booth Coeliac disease and malignancy. Lancet 1983; 1:111-115.
CE, et al. a TCC.
1 5.
Rubesin SE, Herlinger H, Saul SH, Grumbach K, Laufer I, Levine M. Adult celiac disease and its complications. RadioGraphics 1989; 9: 1045-1066.
16.
ZornozaJ, trointestinal
to dissemi-
lym-
Dodd GD. Lymphoma ofthe gastract. Semin Roentgenol 1980;
1S:272-287.
998
U
RadioGrapbics
U
Rubesin
et al
Volume
10
Number
6
The
authors
Hodgkin system cases
present
a simplified
radiographic
lymphoma involving is based on radiographic of
lymphoma
the small findings
involving
the
small
classification of nonintestine. The classification in 22 pathologically proved
bowel
and
consists
of
three
major forms: primary, lymphoma complicating celiac disease, and mesenteric nodal. In this series, small bowel lymphoma was evenly distributed in the jejunum and ileum. The most common radiographic patterns were circumferential lesion (seven cases) cavitary lesion (four cases) and mesenteric nodal disease invading the small bowel (seven cases) Obstructive symptoms were usually encountered with the mesenteric nodal form. Lymphoma complicating celiac disease was typified by multiple, thickened, nodular folds involving a segment of proximal small intestine. ,
,
.
U INTRODUCTION Small bowel lymphoma either by gastrointestinal 20% of primary
is defined symptoms
tract tumor that is manifested mass (1 -3) Approximately tumors in the small bowel are lymphoma (4,5). Almost are non-Hodgkin lymphoma (6) Most of these tumors a diffuse histologic pattern, and are composed of large
malignant
all small bowel lymphomas are of B cell origin, have lymphoid cells. In this article, we correlate Hodgkin lymphoma involving
as an alimentary or an abdominal
.
.
the radiologic and pathologic the small bowel. We present
manifestations a simplified
of nonclassifica-
tion system for non-Hodgkin lymphoma involving the small bowel, in which the disease is classified into three major forms: a primary form, lymphoma complicating celiac disease, and a mesenteric nodal form. Each of these forms has distinct radiographic patterns. Recognition of the type of bowel involvement may direct further workup of the patient or help in treatment planning. Abbreviation: Index
H-E
terms:
Intestinal
RadioGraphics I
From
the
1990;
the
hematoxylin-eosin
Departments
University
neoplasms,
March
quests
to S.E.R.
27,
2 Current
address:
Current ‘C RSNA,
address: 1990
1990; X-Ray
#{149} Intestinal
neoplasms,
staging,
74.34
Lymphoma,
staging,
#{149}
74.34
10:985-998 ofRadiology
of Pennsylvania,
ceived
74.34
revision
Spruce
requested
Department,
Department
(S.E.R.,
3400
Stirling
of Pathology,
A.M.G.,
H.H.,
KG.,
St, Philadelphia, April Royal Chester
18 and
M.S.L.,
PA I 9 1 04 received
Infirmary, County
IL.) .
and
From
the
Pathology 1 989
May 9; acceptedJune Livilands,
Hospital,
Stirling, West
Chester,
(MB., RSNA 14.
S.H.S.),
scientific
Address
Hospital assembly.
reprint
of’ Re-
re-
Scotland. Penn.
985
Table 1 Clinical Summary
of Patients
with
Non-Hodgkin
Lymphoma
ing
Involv
the
Sm all Bowel
Symptoms Form of Involvement
Abdommat Pain
Signs
Average Age (y)
Primary Comp!icating celiacdisease Mesenteric nodal
11
63
6
2
3
2
4
61
1
0
0
0
7
43
3
0
5
5
5
All
22
56
10
2
8
7
6t
A
t
See discussion of individual Excludes data from patients
Fever
Nausea
cases in text and in figure with celiac disease.
Table 2 Number
and
follow-through enema (CT)
0
0 7
4 8
Size
of Lesions No. of Patients
Average Length (cm)
Range (cm) 4-30 4-13
Total
22
12
4-30
enced
with symptoms
,
tions, 1 1 small bowel computed tomographic
4
13 8
of small bowel disease. The disease was confirmed with exploratory laparotomy in 20 patients (with bowel resection in 1 9) endoscopic biopsy and autopsy in one, and autopsy alone in one. Fif-
teen small bowel
4
19 3
We based our classification system on data from 22 adults with pathologically proved non-Hodgkin lymphoma involving the jejunum and ileum, who presented at the Hospital of the University of Pennsylvania and the Philadelphia Veterans Administration Hospi. tal from 1977 to 1989. We included only those patients for whom adequate radiologic studies and surgical or autopsy proof were available. We excluded (a) all patients with disseminated lymphoma (involving the spleen, liver, small bowel, and lymph nodes) at the time of initial diagnosis and (b) all patients who had a history of nodal lymphoma
presented
*
3
Solitary Multifocal
POPULATION
who subsequently
7
legends.
Type of Involvement
U CLINICAL
Vomiting
Abdomma! Mass
Weight Loss
Duration (mo)
No. of Patients
examinastudies, and studies were
13
reviewed.
tients.
by approximately one-third of the paPyrexia was seen in only two patients.
S Predisposing Conditions Non-Hodgkin lymphoma of the small bowel has been associated with acquired immunodeficiency syndrome (AIDS), celiac disease, systemic lupus erythematosus, Crohn dis-
ease, and chemotherapy
undergone
radiation
(7,8) Two systemic
of our lupus
.
patients had long-standing erythematosus. One patient tory of mediastinal Hodgkin
had a 6-year hisdisease
therapy,
and
had
chemotherapy,
and autologous bone marrow transplantaiion. No patients with AIDS or Mediterranean lymphoma were seen in our series.
. RADIOGRAPHIC FINDINGS Lymphoma involving the small intestine tends to involve longer segments of bowel comparison with primary adenocarcinoma. In our series, the average length of diseased bowel was 1 2 cm. Although small bowel non-Hodgkin
lymphoma
is usually
in
a solitary
lesion,
multiple sites are involved in 10%25% of cases (6) In our series, three of 22 patients had multiple lesions (Table 2). In children and young adults, lymphoma primarily affects the ileocecal region (5,6). In adults, most investigators have found that .
.
Symptoms
and
Signs
All patients presented with symptoms related to the small bowel. Abdominal pain was the most frequent symptom, experienced by about half the patients (Table 1) Nausea, vomiting, and weight loss were also experi.
986
#{149}Ra4ioGrapbks
#{149} Rubesin
et al
the ileum, especially the distal ileum, the most frequent site of tumor (6,9)
Volume
10
was .
In our
Number
6
Table
3 of Non-Hodgkin
Distribution Bowel Form
Lymphoma
Proximal
Primary Complicating celiac disease Mesenteric nodal All Note
in the Small
-Numbers
represent
Middle
Distal
5
3
3
3 1
1 5
0 1
9
9
4
number
of patients.
I
Figure 1. Circumferential lymphoma. A 79-year-old woman with a right upper quadrant mass underwent a small bowel followthrough examination. Spot radiograph from that examination shows a 1 2-cm-long lesion with a mildly increased luminal diameter, irregular contour, and nodular surface pattern (arrow) At surgery, a lymphoma of the ileum was found focally invading the small bowel mesentery. Diagnosis: diffuse, large cell lymphoma. .
masses and sprue pattern. However, on the basis of our experience, we have modified this traditional classification into three categories: (a) primary form, (b) lymphoma complicating celiac disease, and (C) mesen-
teric
nodal
form.
. Primary Form Eleven of our patients had the primary form of small bowel lymphoma. In this pattern, the bulk of the lymphomatous tumor lies within
the
intestinal
direct extension tery and spread
wall,
but
into the small to the regional
often
bowel lymph
Tumor
however,
primary
phoma was evenly the small intestine with celiac disease, volved
the
proximal
small
distributed (Table 3) lymphoma jejunum
bowel .
lym-
throughout In patients usually in(Table
3).
The traditional radiographic classification of small bowel lymphoma (1 0, 1 1) has five categories: (a) multiple nodular defects, (b) infiltrating form, (C) polypoid form, (d) endoexoenteric
formation, mesenteric
November
form
with
cavitation
and
is
mesennodes.
spread to the liver, spleen, bone and distant lymph nodes may occur er. The two major radiographic patterns
marlatare a
circumferential
and a
row, series,
there
cavitary
lesion
lesion (four
(seven
patients)
patients).
Circumferential Lesion-This pattern is characterized by a sharply circumscribed annular tumor involving a relatively long segment of small bowel (Fig 1). Submucosal infiltration by tumor causes effacement of mu-
fistula
and (e) predominantly invasive form with large extraluminal
1990
Rubesin
et al
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Figure 2. Circumferential lymphoma. A 79-year-old man had a 2-year history of abdominal pain suggestive of ischemia. (a) Spot radiograph from the single-contrast phase of a small bowel enema examination shows an abrupt, annular lesion 6 cm in length with effaced mucosal folds (arrow) (Reprinted, with per. mission, from reference 8.) (b) Surgical specimen shows a sharply circumscribed lesion (arrow) with an ulcerated mucosal surface and extension into the mesentery. (c) CT scan reveals a small bowel loop with a thickened wall (arrow) (d) Low-power photomicrograph (hematoxylin-eosin [H-EJ stain) of a specimen slice. At the margin of the specimen, submucosal tumor (T) has a sharp margin and extends into the muscularis propria (arrow). Diagnosis: diffuse, large cell lymphoma. .
.
988
#{149}RadioGrapbics
U
Rubesin
et al
Volume
10
Number
6
a.
b. Figure 3. Circumferential lymphoma with mild dilatation. A 70-year-old man had abdominal pain, anemia, and heme-positive stool. (a) Spot radiograph from a small bowel follow-through examination shows a 14-cm-long annular lesion (arrows) with complete effacement of mucosal folds and mild lu-
minal
dilatation.
(b) CT scan demonstrates
a well-
circumscribed lesion with a markedly thickened (arrows) . (c) Surgical specimen shows a well-circumscribed, bulky tumor with a thickened wall rows) . At surgery, tumor invasion of the bladder
sigmoid ic nodal large from
mesentery
involvement cell lymphoma. reference 8.)
was found, was seen. (Reprinted,
but no local
wall (arand
mesenter-
Diagnosis: diffuse, with permission,
c.
cosal folds (Fig 1) may tact mucosa tumor. The narrowed, dilatation) mon because
November
(Fig 2) (1 2) Mucosal nodularity reflect mucosal ulceration or inoverlying nodular submucosal luminal diameter may be slightly normal, or widened (aneurysmal (Fig 3). Obstruction is uncomthe infiltrating tumor weakens .
1990
the muscularis propria of the bowel wall and does not elicit a desmoplastic response. Only one of seven patients with this pattern had clinical and radiographic signs of obstruction.
Rubesin
et al
#{149}RadioGrapbics
#{149}989
-.
a.
ITT
b.
Figure 4. Cavitary lymphoma. A 22-year-old woman with an 8-year history of systemic lupus erythematosus presented with abdominal pain and fever attributed to small bowel ischemia. (a) Spot radiograph from a small bowel followthrough examination shows a small ulcer (arrow) on the mesenteric border associated with slightly thickened folds. This lesion was not described on the initial radiographic report. (b) Eleven weeks later, the patient presented with severe abdominal pain,
tenderness,
and
fever.
Spot
radiograph
from
a small bowel enema study shows a large ulcer (short arrows) irregular nodules (curved arrow), and thickened folds (long arrows) (c) At surgery, a small intestinal tumor was found that had focal,
.
ly perforated
into
into a mesenteric
mesenteric
lymph
fat and
node.
Surgical
had spread
specimen
shows a cavity (C ). Diagnosis: diffuse, large cell lymphoma. (Fig 4a and 4c reprinted, with permission,
from
reference
8.)
C-
Cavitary Lesion.-Cavitary lesions second most frequent radiographic of primary small bowel non-Hodgkin phoma. Ulceration initially extends intramural portion of the tumor (Fig advanced lesions extending into the
are the pattern lyminto the 4) In mesen.
tei-y, ulceration may result in cavitation of the bulk of the tumor. If the cavitated mesenteric portion of the tumor perforates into the mesentery, adherence of small bowel loops and intraloop abscess formation may occur (Fig 5) Fever is an uncommon clinical finding in non-Hodgkin lymphoma involving the small bowel. In our series, the two patients with fever had cavitary lesions and confined perforations. .
990
U
Ra4ioGrapbics
U
Rubesin
et al
Volume
10
Number
6
.,
:.‘
.c
‘.
..
..-
Figure 5. Cavitary lymphoma with focal perforation and intraloop abscess formation. A 74-yearold woman had a 5-month history of abdominal pain and weight loss and an abdominal mass. (a) Spot radiograph from a small bowel enema study shows a large, barium-filled cavity (C) along the mesenteric border of several bowel loops. (b) CT scan reveals contrast material (C) filling the lumen of a thin-walled cavitary mass (arrows) (c) Gross specimen of a 1 6-cm mass found at surgery. The mass consists of a small bowel lymphoma, which had extended into the mesentery, cavitated, and perforated, forming a mesenteric abscess (A ) surrounded by adherent .
‘
4.;
.-‘I%,
,
-i
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.:
‘
. .
,
, ,
.:
‘
.
.
.
.
.
.
,..
, -
,
..
-. - -
.
.
. ‘
. ‘ .‘
small
bowel
nodes
were
surgical
from v
‘
November
specimen
shows
an ulcer
surface
extending
Low-power
(Fig
5a and
from reference
1990
of 1 9 mesenteric
by lymphoma.
photomicrograph
lymph
(d) Opened (U) viewed into the cavi(H-E)
shows
tumor (T) extending from mucosal surface to the lumen of the cavity (C ). Diagnosis: diffuse, large cell lymphoma with T cell surface antigen markers.
e.
Three
the luminal
ty. (e) -
1oops.
infiltrated
Sc reprinted,
with
permission,
8.)
Rubesin
et al
U
Ra4ioGrapbics
U
991
Figures
6, 7. (6) Lymphoma complicating celiac disease. A 69-year-old woman with long. standing celiac disease presented with recurrent symptoms despite dietary restriction. Spot radiograph from a small bowel enema study shows thick, nodular
folds
(arrows)
in a 1 5-cm
loop
:‘ .
.. ,f’,
-.
of jeju,
num.
Diagnosis:
diffuse,
large
cell
#{149}1’
lymphoma.
(7) Subtle lymphoma complicating celiac disease. A 53-year.old man complained of acutely increasing diarrhea and weight loss; 6 months previously, celiac disease had been diagnosed at jejunal biopsy.
(a)
Spot
radiograph
from
a small
bowel
en-
ema study shows subtle nodular folds (arrows) the jejunum. (b) Medium-power photomicrograph (H-E) of endoscopic biopsy specimen shows villous atrophy (arrowheads) ma infiltrating the lamina propria cosa (S ) . Diagnosis: diffuse, large
with
T cell
surface
antigen
in .n’
and lympho) and submucell lymphoma
(L
markers. ..-..c.
S Lymphoma Celiac Disease
Complicating
.
,
.
U
RadioGrapbics
U
Rubesin
et al
‘4.
‘.
S
‘
S
Four patients in our series had lymphoma complicating celiac disease. Although it is a form of primary small bowel non-Hodgkin lymphoma, lymphoma complicating celiac disease is characterized by a different clinical history, location, and radiographic appearance Whereas most cases of small bowel non-Hodgkin lymphoma are of B cell origin (9) most, if not all, cases of lymphoma complicating celiac disease are of T cell origin (1 3) Patients with the latter disease usually have a long history of celiac disease and sub-
992
,.-,
%
S
-
‘
_4
,
.5’
‘1
7b.
sequently develop diarrhea, malabsorption, and weight loss despite continued dietary restriction (1 4) In some patients, initial diagnosis of celiac disease and coexistent lymphoma may be made at an elderly age. Two of our four patients had a 6-month history of severe malabsorption, weight loss, diarrhea, and no previous history of celiac disease. .
Volume
10
Number
6
Figures
8, 9.
(8) Mesenteric nodal lymphoma invadAn abdominal mass was palpated in a 55-year-old man. Spot radiograph from a small bowel enema study shows extrinsic mass impression, primarily on the mesenteric border of small bowel (large arrow); narrowing of the lumen (small arrows) ; and dilatation of proximal small bowel, a finding indicative of obstruction. At surgery, a diffuse, large cell lymphoma of the mesentery was found encasing the small intestine. (9) Mesenteric nodal lymphoma. A 52-year-old woman presented with crampy abdominal pain and vomiting. ( a) Overhead radiograph from a small bowel enema study shows separation of small bowel loops; abrupt angulation of loops (large arrow) ; tethering of folds (small arrows) ; and dilatation of proximal versus distal small
ing small bowel.
bowel, a finding indicative of (b) CT scan shows a mesenteric the mesenteric border of small rows) and focal circumferential around
fuse,
a small
large
cell
bowel
loop
partial
obstruction.
mass (m ) compressing bowel loops (small arextension of tumor
(large arrow).
Diagnosis:
dif-
lymphoma.
8.
9a.
9b.
Non-Hodgkin lymphoma in celiac disease usually involves the proximal small intestine, which is the site of the greatest villous damage and inflammation. Enlarged, nodular folds involve a variable length of small intes-
tine (Fig 6). The radiographic phoma complicating subtle,
ema
even
manifestations celiac disease
on images
from small bowel en7) (1 5) Radiographof lymphoma from ulcer-
examinations
(Fig
Ic differentiation
.
aiive jejunoileitis complicating ease may be impossible (15). .
Mesenteric
In most
teric
series,
lymph
Nodal lymphoma
nodes,
with
1990
celiac
dis-
Form arising
direct
into the small bowel, is classified bowel lymphoma (6). However,
November
of lymmay be
in mesen-
extension
that mesenteric nodal lymphoma with direct invasion of the small bowel is a distinct radiographic entity. The seven patients in our series with this form of lymphoma underwent exploratory laparotomy, five for obstructive symptoms and two for an abdominal mass. In each patient, large mesenteric masses abutted, displaced, and focally invaded the small bowel.
In six of the seven patients, no other tumor was seen. One patient had focal, retroperitoneal lymphadenopathy. The radiographic findings of mesenteric nodal lymphoma consist of mass effect along the mesenteric border of the small intestine (Fig 8) angulation of small intestinal loops (Fig 9) spiculation and tethering of the lu,
,
as small we believe
Rubesin
et al
U
Ra4ioGrapbics
U
993
a.
b.
d.
C-
Figure 10. Mesenteric nodal lymphoma. A 32-year-old woman had a left upper quadrant mass detected at routine physical examination conducted S months after cesarean section. (a) Overhead radiograph from a small bowel follow-through examination shows separation of proximal jejunal loops and extrinsic mass effect along the mesenteric border of small bowel (open arrows) and stomach (solid arrow) Focal thick.
ening
of jejunal
folds
(curved mass (M
arrows)
is seen
at the
site
of bowel
wall
invasion.
(b)
CT scan
demonstrates
a large mesenteric ) (c) Low-power photomicrograph (H-E) of specimen obtained where tumor either abutted or was adjacent to small bowel shows lymphoma (L ) extrinsic to the muscularis propria (M ) of the bowel. (d) Medium-power photomicrograph (H-E) of specimen from the site of thickened folds shows lymphoma (arrow) focally invading through the muscularis propria (M ) into the submucosa (S
994
U
RadioGraphics
) Diagnosis:
diffuse,
.
U
Rubesin
.
large
cell
et al
lymphoma.
Volume
10
Number
6
“3
M
Figure 11. Mesenteric nodal lymphoma. A 23year-old man had a 6-year history of mediastinal Hodgkin disease treated with radiation therapy, chemotherapy, and autologous bone marrow
:;.i
transplantation. He had a stable (a) Spot radiograph from small
r
A
mediastinal mass. bowel follow-
through examination shows a smooth, extrinsic mass impression on the mesenteric border (arrows) of a loop of the midportion of the small
bowel.
(b)
Four months
later,
the patient
com-
plained of vomiting. Spot radiograph from small bowel follow-through examination shows enlargement of the mesenteric mass, with spiculalion and tethering (arrows) of the mesenteric bor-
der of the small C-
minal small folds
contour, and variable narrowing of the intestinal lumen. Thickened nodular in the region of tethering indicate areas
of tumor invasion of the small bowel (Fig 1 0) In one patient, radiologic studies showed clear progression from an extrinsic
bowel,
and narrowing
of small
bowel loops. Dilatation of the proximal small bowel was seen. (C) CT scan obtained at the same time as b shows a large mesenteric mass (M ) . At surgery, there was partial small bowel obstruction and a mesenteric mass focally invading the serosa of the small bowel. Diagnosis: diffuse, large cell lymphoma with histologic characteristics distinct from those of Hodgkin disease.
.
mesenteric
mass
tine to a mesenteric structing the small
November
1990
compressing
mass bowel
the
small
intes-
invading and ob(Fig 11).
Rubesin
et al
U
RadioGraphics
U
995
a.
b I
.-
‘-
.
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,
:
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-
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.
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,
d.
C.
Figure
12.
Target
lesions.
A 55-year-old
woman
with
a 3-year
history
of lymphoma
involving
axillary
and
ingumnal lymph nodes complained of abdominal pain. (a) Spot radiograph demonstrates two sharply circumscribed lesions with smooth surfaces and central ulceration (arrows) along the greater curvature of the stomach. (b) Another spot radiograph shows numerous target lesions (arrows) in the duodenum. p = papilla of Vater. (c) Spot radiograph from small bowel follow-through examination shows a target lesion (arrow) in the jejunum. (d) At surgery, numerous nodules were found in the jejunum. Medium-power photomicrograph (H-E) of the pathologic specimen shows submucosal tumor (T) below the muscularis mucosae (arrow) Tumor focally invades the mucosa (M ) and underlies a large mucosal ulcer (U) DiagflO5iS: disseminated large cell lymphoma. (The patient was not included in our series because of the disseminated nature of her disease.)
.
.
Unusual
.
Radiographic
Patterns
Target Lesions.-Submucosal masses with central ulceration (target lesions) are an Uncommon appearance of non-Hodgkin lymphoma involving the small intestine. We have seen only one case of lymphomatous target
the
lesions
case
in the
was
not
small
included
bowel.
in this
However,
series
be-
cause the non-Hodgkin
U
Ra4ioGrapbics
U
Rubesin
et al
nodal
SmallNodules.-Although mu!nodules involving long segments of the bowel have been reported as a comradiographic manifestation of non-
Numerous
tiple small mon Hodgkin
countered
996
patient had disseminated lymphoma (Fig 12).
lymphoma
this
pattern
(1 6),
we
during
Volume
have
the
10
not
past
en-
12
Number
6
13.
Figures
13, 14.
lar pattern.
(13)
graph
from
small
study
shows
3-5
Diffuse Spot
bowel
numerous
mm in diameter
small
bowel
loops.
nodu-
radio-
enema nodules
carpeting Nodules
are
more conspicuous than thickened folds. (Courtesy of Dean D. T. Maglinte, MD, Methodist Hospital, Indianapolis.) (14) Alpha chain disease (Mediterranean lymphoma) Overhead radiograph shows numerous small nodules (arrow) distorting the entire surface of the small intestine. No narrowing is seen. (Courtesy of Emeric Lax, MD, Hadassah University Hospital, Jerusalem; reprinted, with permission, from reference 1.)
.
.;:v’
14.
patients were not included cause they were from other
two These in our series beinstitutions. We
are uncertain
nodular
years.
For
examples
represents volving
November
completeness,
we
of this pattern
(Figs
if the diffuse (a)
multiple
illustrate
13
,
1 4)
pattern
disseminated lymphoma organ systems, lymph
1990
.
nodes, and small bowel; (b) lymphoma associated with immunodeficiency states; or (c) Mediterranean lymphoma. Patients with Mediterranean lymphoma (alpha chain disease, immunoproliferative
in-
Rubesin
et al
U
Ra4ioGrapbics
U
997
small
intestinal
disease)
present
with
.
tered
any patients
with
this disease
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