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Primary follicular lymphoma of the pancreas: A rare tumour mimicking pancreatic carcinomaSugunah SALLAPAN1, Nor Zailin ABU BAKAR2, Razman JARMIN3, Noraidah MASIR1, Fazarina MOHAMMED1
Departments of Pathology1, Radiology2 and Surgery3, Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Kuala Lumpur, Malaysia.
Abstract
Introduction: Primary pancreatic lymphomas are extremely rare. Clinically, primary pancreatic lymphoma mimics symptoms of carcinoma of the pancreatic head. Clinical and radiological features may overlap with other pancreatic conditions such as carcinoma, neuroendocrine tumours and autoimmune pancreatitis. Case Report: We report a case of a 75-year-old man who presented with symptoms of obstructive jaundice. Ultrasonography and computed tomography (CT) showed an ill-defined lobulated soft tissue lesion at the head/uncinate process of the pancreas measuring 4.5 x 4.9 x 5.8 cm. The patient underwent pancreaticoduodenectomy for suspected pancreatic head/uncinate process carcinoma. Histopathology and immunohistochemical assessment of the pancreatic lesion established the diagnosis of a low-grade follicular lymphoma. Discussion: Clinical and imaging features of primary pancreatic lymphoma may often overlap with pancreatic carcinoma. There is a value of obtaining preoperative tissue diagnosis such as tissue biopsy and fine needle aspiration (FNA) cytology with or without flow cytometry to make an accurate diagnosis of non-Hodgkin lymphoma and alleviate the need of more radical surgery in pancreatic lymphoma.
Keywords: Non-Hodgkin lymphoma, primary pancreatic lymphoma (PPL), follicular lymphoma, pancreas, obstructive jaundice
Address for correspondence: Dr Fazarina Mohammed, Department of Pathology, Faculty of Medicine, UKM Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, Cheras 56000, Kuala Lumpur, Malaysia. Tel: 03-91459482; Fax: 03-91459485. Email: [email protected]
CASE REPORT
INTRODUCTION
Gastrointestinal lymphomas constitute 10-15% of all non-Hodgkin lymphomas and 30-40% of all extranodal lymphomas.1,2 Gastrointestinal non-Hodgkin lymphoma (NHL) usually involves the stomach and the small bowel. Rarely, it can also present as a pancreatic mass. Most cases of pancreatic non-Hodgkin lymphoma are part of a disseminated disease. Primary pancreatic lymphoma is rare and accounts for less than 1% of all primary pancreatic tumours.3
Diagnosis of primary pancreatic lymphoma requires the absence of palpable superficial lymphadenopathy or mediastinal nodes enlargement, and normal leukocyte count. Furthermore during laparotomy pancreatic mass predominates and if grossly-involved lymph nodes are seen they are usually confined to the peripancreatic region with no hepatic or splenic involvement.4 Clinical presentation of primary pancreatic lymphoma mimics pancreatic
carcinoma, for example patient presents with abdominal pain, weight loss, vomiting, jaundice, night sweats and fever.5 However, CA 19.9 level is usually normal unless biliary obstruction is present.6 Clinical and imaging features of primary pancreatic lymphoma may overlap with other pancreatic conditions such as carcinoma, neuroendocrine tumours and autoimmune pancreatitis. Therefore, histological diagnosis is mandatory because of different prognosis and therapeutic approaches of these conditions. We report a case of primary pancreatic lymphoma in an elderly man presented with symptoms of obstructed jaundice mimicking pancreatic carcinoma.
CASE REPORT
A 75-year-old man presented with jaundice for two weeks. He denied having fever, abdominal pain, and loss of appetite or weight. His bowel and urine output were otherwise normal. He
Malaysian J Pathol 2018; 40(3) : 359 – 371
Malaysian J Pathol December 2018
360
had hypertension and bilateral glaucoma. Initial ultrasound of hepatobiliary system as a workup for jaundice showed an ill-defined, hypoechoic lesion at the head of pancreas measuring 4.0 x 4.5 cm with both intrahepatic and extrahepatic ducts dilatation. Subsequent abdominal computed tomography (CT) scan revealed an ill-defined lobulated soft tissue lesion at the head/uncinate process of the pancreas measuring 4.5 cm x 4.9 cm x 5.8 cm causing biliary tree obstruction suggestive of pancreatic head/uncinate process carcinoma (Fig. 1). Subcentimeter porta hepatis lymph nodes measuring 0.9 cm in largest diameter were also seen. The liver and spleen were unremarkable. Chest radiograph showed no evidence of lung or mediastinal mass. His liver function test showed mild to moderate derangement with obstructive pattern (Total Bilirubin and Direct Bilirubin: 172 µmol/L and 132.6 µmol/L respectively [Normal Total Bilirubin: <20.5 µmol/L, Direct Bilirubin: <5 µmol/L]), Alkaline Phosphatase (ALP): 276 U/L [Normal ALP: 45-115 U/L] and Alanine Transaminase (ALT): 151 U/L [Normal ALT: 7-55 U/L]) while his white blood cells count, serum CA 19.9 marker and amylase were within normal limits. Based on the clinical and radiological findings which support the diagnosis of pancreatic carcinoma, the patient underwent pancreaticoduodenectomy (Whipple procedure). Intraoperative finding showed a mobile head of pancreas tumour, a large mesenteric node measuring 4 x 5 cm and multiple subcentimeter peripancreatic and portal nodes. The common bile duct and common hepatic duct were dilated. The mesenteric lymph node was removed en bloc together with the resected specimen.
The resected pancreas and duodenum revealed a 5 cm, irregular yellowish-to-tan mass within the pancreatic head (Fig. 2). The tumour surrounded the main pancreatic duct, distal common bile duct but did not appear to obliterate the duct. Enlarged peripancreatic and mesenteric lymph nodes were readily identified: the largest measured 4.5 cm in greatest dimension. Microscopically, the pancreatic mass showed infiltration by neoplastic lymphoid cells forming follicular pattern with no reactive lymphoid tissue seen. The neoplastic follicles are composed of predominantly centrocytes characterised by small to medium sized cells with hyperchromatic nuclei, inconspicuous cleaved nucleoli, and scanty cytoplasm. Few scattered centroblasts characterised by large cells with vesicular nuclei and prominent peripheral nucleoli are seen with a count of 4 centroblasts per high power field. The mesenteric lymph node showed diffuse effacement of the normal lymph node architecture with infiltration by similar neoplastic lymphoid follicles as the pancreas. The remaining lymph nodes showed reactive hyperplasia. Immunohistochemical studies revealed that the tumour cells express CD20, CD10, and BCL2. CD23 highlights the follicular dendritic meshwork. They were negative for CD3, CD5, and Cyclin D1. Ki-67 showed a proliferative index of 20% in the neoplastic follicles (Fig. 3). The overall findings were consistent with low-grade follicular lymphoma, WHO grade I with involvement of mesenteric lymph node. Radiologic imaging showed no evidence of extra-abdominal disease.
FIG. 1: (A) Computed tomography (CT) scan revealed an ill-defined lobulated soft tissue lesion at the head/uncinate process of the pancreas measuring 4.5 cm x 4.9 cm x 5.8 cm. The mass is isodense to the rest of the pancreas in the portovenous phase. There is no clear fat plane with the D2 of the duodenum laterally (arrow). (B) Dilatation of common bile duct and intrahepatic ducts are evident.
361
PANCREATIC FOLLICULAR LYMPHOMA
DISCUSSION
Lymphoma originating from pancreas comprises only 0.6% of total cases of extranodal malignant lymphoma.7 The most common histologic type of the pancreatic lymphoma is diffuse large B-cell lymphoma, while follicular lymphoma is rare.8 An extensive review of the international literature has revealed a total of 102 patients with Non-Hodgkin lymphoma primarily involving the pancreas with majority of cases being diffuse large B-cell lymphoma (Table 1).4,9-38 Only 9 cases were follicular lymphoma.18,19,37
The accurate diagnosis of primary pancreatic lymphoma may be missed when the tumour is confined to the pancreas and surrounding peripancreatic lymph nodes. A study attempted to elaborate the distinguishing features between pancreatic carcinoma and pancreatic haematologic malignancy. The study found that features more often seen in patients with haematologic malignancies includes young age at presentation, large tumour size, low preoperative CA19.9 level, history of a pre-existing haematological malignancy, presence of B symptoms, absence of jaundice or diabetes mellitus.39 In this case however, the patient is elderly, presented with obstructive jaundice and a large mass in the head of pancreas. This led
to high suspicion of pancreatic adenocarcinoma instead of primary pancreatic lymphoma. Primary pancreatic lymphoma is less likely to present with jaundice and mass at head of the pancreas thus reducing the suspicion of primary pancreatic lymphoma.40
Albeit gastrointestinal lymphoma has a wide variety of imaging appearances, one study have shown that certain findings such as bulky mass or diffuse infiltration with preservation of fat planes and no obstruction, multiple site involvement, and associated bulky lymphadenopathy can strongly suggest the diagnosis.41 According to two other studies, there were radiological findings that may favour primary pancreatic lymphoma instead of pancreatic adenocarcinoma such as bulky localised pancreatic head tumour, no significant pancreatic duct dilatation, lack of calcification or necrosis, no enlarged lymph nodes below the level of the renal veins, and no retroperitoneal, hepatic, or splenic involvement.42,43 In contrary, two studies have shown that abdominal CT is not a definitive method in distinguishing pancreatic carcinoma from pancreatic haematologic malignancy.44,45
This further implies the difficulty in preoperative diagnosis of primary pancreatic lymphoma. In our patient, the clinical and imaging features are
FIG. 2: Grossly, a firm, yellowish-to-tan tumour was seen at the head of pancreas (arrow). The common bile duct was dilated (arrowhead).
Malaysian J Pathol December 2018
362
FIG. 3: (A) Microscopic examination: Haematoxylin & eosin staining showing pancreatic infiltration by poorly defined neoplastic lymphoid follicles (H&E, x4). (B) Medium sized neoplastic lymphoid cells expressing CD20 (x10). (C) The Ki-67 proliferative index is 20% (x10). (D, E, & F) The neoplastic lymphoid cells express CD23, CD10, and BCL2 (x10).
rather inconclusive for preoperative diagnosis of pancreatic lymphoma as he presented with symptoms of obstructive jaundice and bulky lesion in pancreatic head/uncinate process causing biliary tree obstruction. There were no pancreatic duct dilatation, calcification, or hepatic and splenic involvement seen. Only subcentimeter porta hepatis lymph nodes were found. These findings within his age group are more suggestive of pancreatic carcinoma leading the primary team to proceed with surgical resection. Haematological malignancies are generally treated medically, with surgical management limited to cases necessitating secondary
symptom control. Therefore, preoperative tissue diagnosis would be useful to prevent unwarranted radical surgery in suspected cases involving haematological malignancies. It has been reported that endoscopic ultrasound-assisted fine needle aspiration (EUS-FNA) may be utilised in the diagnosis of pancreatic carcinoma and pancreatic haematologic malignancy.46 A retrospective study showed that the diagnostic accuracy of fine needle aspiration (FNA) with cytology for primary pancreatic lymphoma is improved greatly with the addition of flow cytometry and immunohistochemistry.40 This study shows that cytology alone made the final diagnosis of lymphoma in only 28% of the patients versus
363
PANCREATIC FOLLICULAR LYMPHOMA
TABL
E 1:
Sum
mar
ies
of li
tera
ture
rev
iew
s on
pri
mar
y pa
ncre
atic
lym
phom
aA
utho
rsYe
arN
o of
Cas
es/
Gen
der/
Age
Clin
ical
pr
esen
tatio
nL
ocat
ion
of
tum
our
in
panc
reas
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Shta
mle
r et
al.9
1988
Fem
ale/
31D
iarr
hoea
, vo
mitt
ing,
up
per
abdo
min
al
pain
, and
w
eigh
t los
s
Hea
dD
iffus
e hi
stio
cytic
ly
mph
oma
CT:
Enl
arge
d liv
er w
ith se
vere
di
lata
tion
of th
e in
trahe
patic
bi
le d
ucts
. Spa
ce o
ccup
ying
le
sion
in h
ead
of th
e pa
ncre
as
mea
surin
g 50
x 8
0 m
m in
size
. N
o en
larg
ed re
trope
riton
eal
lym
ph n
odes
.
CT
– gu
ided
ne
edle
bio
psy
was
per
form
ed
with
inco
nclu
sive
di
agno
sis.
PD +
CM
TC
R +
Sec
ond
surg
ery
5 m
onth
s la
ter f
or ru
ptur
ed
panc
reat
ic
pseu
docy
st
Web
b et
al.10
1989
4 m
ales
and
5fe
mal
e/49
-76
Wei
ght l
oss,
jaun
dice
, ab
dom
inal
pa
in, g
astri
c ou
tlet
obst
ruct
ion
(3)
Not
sp
ecifi
edD
iffus
e hi
stio
cytic
ly
mph
oma
(6),
Mix
ed
lym
phoc
ytic
hi
stio
ctic
cel
l ly
mph
oma
(2),
Diff
use
lym
phoc
ytic
ly
mph
oma
(1)
CT:
Pan
reat
ic m
ass r
angi
ng
5 –
10 c
m, p
eria
ortic
lym
ph
node
s enl
arge
men
t (6)
, and
C
BD
and
/or i
ntra
hepa
tic
dila
tatio
n (5
)
Rad
iolo
gica
lly
guid
ed ti
ssue
bio
psy
(4),
perip
hera
l ly
mph
nod
e bi
opsy
(1
), an
d la
paro
tom
y (4
)
PD (1
) +
CM
T (9
)C
R(6
) +
Dea
ths (
3)
Hira
baya
shi
et a
l.1119
91M
ale/
74Ep
igas
tric
pain
,wei
ght
loss
Bod
y an
d ta
il D
iffus
e no
n-H
odgk
in’s
ly
mph
oma
CT:
Pan
crea
tic m
ass w
ith
invo
lvem
ent o
f per
ipan
crea
tic
fat.
The
perip
ancr
eatic
lym
ph
node
s and
sple
en w
ere
inta
ct.
NA
Parti
al
panc
reat
ecto
my
+ sp
lene
ctom
y
AWD
Joly
et a
l.1219
92Fe
mal
e/23
Jaun
dice
, fev
erH
ead
Non
-Hod
gkin
lym
phom
a,
com
pose
d of
cl
eave
d, la
rge,
B
-cel
ls
CT:
Low
-den
sity
tum
our o
f the
he
ad o
f the
pan
crea
s with
ne
crot
ic c
ente
r.
Not
don
ePD
+ C
MT
Dev
elop
ed m
ultip
le
mes
ente
rican
d m
edia
stin
al
lym
phad
enop
athi
es,
and
pulm
onar
ym
etas
tasi
s. D
ied
of
dise
ase.
Va
n B
eers
et
al.13
1993
5 m
ales
and
3
fem
ales
/ 26
– 7
7
Epig
astri
c pa
in (8
), ja
undi
ce (4
), fa
tigue
(2)
Hea
d (5
), bo
dyan
d ta
il (3
)
Non
-Hod
gkin
B
lym
phom
as o
f lo
w g
rade
(2),
inte
rmed
iate
gr
ade
(2),
high
gr
ade
(4)
CT:
Tw
o pa
ttern
s wer
e ob
serv
ed; l
arge
infil
tratin
g le
sion
with
poo
rly d
efine
d co
ntou
r and
wel
l del
inea
ted
mas
ses.
The
panc
reat
ic tu
mou
rs
wer
e is
oden
se a
nd h
omog
enou
s on
pre
cont
rast
CT.
The
y ap
pear
he
tero
geno
us in
dyn
amic
CT
(6).
Ret
rope
riton
eal,
mes
ente
ric,
and
perip
ancr
eatic
ly
mph
aden
opat
hies
wer
e ob
serv
ed (5
)
Non
-sur
gica
l bio
psy
of th
e pa
ncre
atic
ar
ea (4
), pe
riphe
ral
lym
ph n
ode
biop
sy
(2),
bone
mar
row
bi
opsy
(1),
surg
ical
bi
opsy
of p
ancr
eas
(1)
NA
NA
Malaysian J Pathol December 2018
364
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Beh
rns
et a
l.419
948
mal
es a
nd 4
fem
ales
/NR
Abd
omin
al
pain
,w
eigh
t los
s, pa
lpab
le m
ass
Hea
d (6
),bo
dy (3
), ta
il (2
), w
hole
of
panc
reas
(1)
DLB
CL
(7),
mix
ed (2
),sm
all c
leav
ed
lym
phom
a (2
)
NA
Preo
pera
tive
tissu
e bi
opsy
(6)
RT (5
), C
MT
(2),
RT+C
MT
(3),
PD (2
)
Die
d of
dis
ease
(1
0)
Bor
row
dale
et
al.14
1994
Mal
e/35
Ep
igas
tric
disc
omfo
rt,
mild
bac
k pa
in, n
ause
a an
d le
thar
gyA
cute
ons
et
of ja
undi
ce,
with
pal
e st
ools
and
dark
urin
e
Not
sp
ecifi
edM
alig
nant
lym
phom
a of
the
B c
ell t
ype
CT:
Mas
s in
the
head
of t
he
panc
reas
mea
surin
g 6
cm, w
ith
inho
mog
eneo
us a
ppea
ranc
e an
d po
orly
defi
ned
mar
gins
. C
ompr
essi
on a
nd d
ispl
acem
ent
of th
e di
stal
CB
D a
nd p
roxi
mal
pa
ncre
atic
duc
t with
dila
tatio
n.
Not
don
eC
MT
NA
Ezza
t et
al.15
1996
4 m
ales
and
1
fem
ale/
38–5
1N
AH
ead
(4),
body
and
ta
il (1
)
DLB
CL
(5)
NA
CT
guid
ed b
iops
y (2
)C
MT
(3),
CM
T+RT
(2),
PD (2
)
CR
(4),
AWD
(1)
Salv
ator
e et
al.16
2000
Mal
e/59
Left
side
d ab
dom
inal
pa
in, e
arly
sa
tiety
Who
le
panc
reas
(d
iffus
e in
volv
emen
t)
DLB
CL
CT:
Spl
enom
egal
y w
ith
mul
tiple
lesi
ons a
nd le
ft up
per a
bdom
inal
per
i-aor
tic
lym
phad
enop
athy
. The
pan
crea
s ap
pear
ed n
orm
al
Tiss
ue b
iops
y du
ring
expl
orat
ory
lapa
roto
my
CM
TN
A
Foro
otan
et
al.17
2001
Fem
ale/
55Ep
igas
tric
pain
, rec
ent
anor
exia
, ea
rly sa
tiety
, w
eigh
t los
s,pa
lpab
le m
ass
Not
sp
ecifi
edD
iffus
e m
ixed
ce
llula
rity
non-
clea
ved
type
no
n-H
odgk
in’s
ly
mph
oma
CT:
Lar
ge p
ara-
aorti
c m
ass
with
het
erog
enou
s,m
ixed
enh
ance
men
t and
en
case
men
t of g
reat
ves
sels
.
Not
don
eSu
rgic
al
tum
our
debu
lkin
g +
CM
T
CR
Nay
er e
t al
.1820
047
mal
es a
nd 1
fem
ale/
35-7
5A
bdom
inal
pa
in (6
), ja
undi
ce,
acut
e pa
ncre
atiti
s,ob
stru
ctio
n,
diar
rhoe
a
Hea
d (7
), bo
dyan
d ta
il (1
)
LBC
L (4
), H
igh-
grad
e B
-cel
l ly
mph
oma
(1),
FC
L (1
),sm
all
lym
phoc
ytic
lym
phom
a (1
),su
spic
ious
(1)
CT:
The
tum
ours
var
ied
in
size
from
2-1
5 cm
in g
reat
est
dim
ensi
on.
Rad
iolo
gic
(USG
/C
T) g
uida
nce
FNA
cy
tolo
gy w
ith fl
ow
cyto
met
ric a
naly
sis
RT+C
MT
(3),
CM
T (4
), N
AC
R (5
)AW
D (1
)N
o in
form
atio
n (2
)
365
PANCREATIC FOLLICULAR LYMPHOMA
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Volm
ar
et a
l.1920
047
mal
es a
nd 3
fem
ales
/46-
86
NA
Hea
d (8
),bo
dy (1
), ta
il (1
)
LBC
L (6
), FC
L (3
), an
dun
clas
sifie
d B
-cel
lly
mph
oma
(1)
NA
FNA
bio
psie
s with
flo
w c
ytom
etry
an
alys
is u
nder
ul
traso
und
(3),
CT
(4),
endo
scop
ic
ultra
soun
d (7
) gu
idan
ce
CM
TD
ied
(1)
PR (2
)C
R (7
)
Ji e
t al.20
2005
Mal
e/46
A
bdom
inal
pa
in, j
aund
ice
Hea
dD
LBC
LC
T: H
ypod
ense
pan
crea
tic
mas
s com
pres
sing
CB
D w
ith
dila
tatio
n of
the
gallb
ladd
er
Not
don
e bu
t in
traop
erat
ive
froz
en se
ctio
n w
as p
erfo
rmed
su
spic
ious
of
ana
plas
tic
carc
inom
a
PDC
R
Arc
ari
et a
l.2120
054
mal
es a
nd 1
fem
ale/
58-7
1 Pa
in a
nd
wei
ght l
oss
Hea
d (5
)LB
CL
(3)
lym
phop
las-
mac
ytic
lym
phom
a (2
)
CT:
Hyp
oden
se/h
ypoe
choi
c pa
ncre
atic
hea
d m
ass r
angi
ng
from
3 to
6.5
cm
FNA
cyt
olog
y w
ith
tissu
e co
re b
iops
y (3
)
PD+C
MT
(2),
CM
T+RT
(2),
CM
T (1
)
CR
(4)
Rel
apse
(1)
Die
d du
e re
curr
ent
chol
angi
tis p
ost
surg
ery
(1) a
nd
liver
cirr
hosi
s (1)
Lee
et a
l.2220
06Fe
mal
e/61
A
bdom
inal
pa
inH
ead
DLB
CL
CT:
Wel
l defi
ned
mas
s loc
ated
at
the
head
of t
he p
ancr
eas
whi
ch w
as sl
ight
ly e
nhan
ced
durin
g th
e ar
teria
l pha
se
Intra
oper
ativ
e fr
ozen
sect
ion
confi
rmed
as
lym
hom
a
Parti
al
exci
sion
of
mas
s + C
MT
CR
Wan
g et
al.23
2006
Mal
e/49
A
bdom
inal
pa
in, j
aund
ice
with
tea
colo
ured
ur
ine
Hea
dB
urki
tt ly
mph
oma
CT:
Sus
pici
ous p
eria
mpu
llary
tu
mou
r with
mild
CB
D
dila
tatio
n.M
RI:
Rel
ativ
ely
clea
rly d
efine
d an
d ho
mog
eneo
us si
gnal
mas
s in
the
panc
reat
ic h
ead
with
bi
liary
dila
tatio
n on
enh
ance
d st
udy.
Endo
scop
ic
guid
ed b
iops
y re
porte
d as
chr
onic
in
flam
mat
ion
PDD
ied
2 da
ys d
ue
to p
ost o
pera
tive
com
plic
atio
n
Lin
et a
l.2420
065
mal
es a
nd 1
fem
ale/
16-6
5Pa
in, m
ass,
wei
ght
loss
, jau
ndic
e,
naus
ea,
vom
iting
Hea
d (3
), bo
dyan
d ta
il (2
),w
hole
of
panc
reas
(1)
B-c
ell l
ymph
oma
(3) a
ndN
on-H
odgk
in B
ly
mph
oma
(3)
CT:
The
tum
ours
wer
e la
rger
th
an 6
cm
(4),
with
alm
ost
hom
ogen
eous
den
sity
and
un
clea
r edg
es. E
nhan
ced
CT
scan
onl
y en
hanc
ed th
e ed
ges
slig
htly
.
EUS-
guid
ed fi
ne-
need
le a
spira
tion
(2)
PD+C
MT
(4),
CM
T+RT
(2)
Die
d (3
)Lo
st to
follo
w
up (2
)C
R a
nd o
n fo
llow
up
(1)
Malaysian J Pathol December 2018
366
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Bas
u et
al.25
2007
Mal
e/42
A
bdom
inal
pa
in, J
aund
ice
Bod
yD
LBC
LC
T: L
arge
, lob
ulat
ed,
hete
roge
neou
sly
enha
ncin
g, so
ft tis
sue
mas
s aris
ing
from
bod
y of
pan
crea
s with
com
pres
sion
of
CB
D.
Truc
ut b
iops
y C
MT+
RTC
R
Liak
akos
et
al.26
2008
Mal
e/65
A
bdom
inal
pa
in,
jaun
dice
,an
orex
ia
Hea
dD
LBC
LC
T: L
arge
het
erog
eneo
us
enha
ncem
ent o
f a la
rge
tum
our
of th
e he
ad o
f the
pan
crea
s, in
con
tact
with
the
supe
rior
mes
ente
ric v
ein
(SM
V),
with
out s
igns
of i
nfiltr
atio
n or
en
case
men
t of t
he v
ein,
or t
he
supe
rior m
esen
teric
arte
ry.
Lim
ited
lym
phad
enop
athy
w
as a
lso
dete
cted
in th
e pe
ripan
crea
tic a
nd th
e pa
ra-
aorti
c re
gion
s.
CT-
guid
ed fi
ne
need
le a
spira
tion
(FN
A) b
iops
y w
as
not d
iagn
ostic
PD+C
MT
Aliv
e
Has
him
oto
et a
l.2720
08M
ale/
50
Jaun
dice
Hea
dD
LBC
LC
T: L
ow-d
ensi
ty m
ass,
10 c
m in
dia
met
er, i
n th
e re
trope
riton
eal s
pace
beh
ind
the
panc
reas
hea
d, d
ista
l bile
duc
t an
d th
e PV
wer
e ob
stru
cted
Not
don
eC
MT+
PDC
R
Sagl
am
et a
l.2820
09M
ale/
20
Wei
ght l
oss,
back
pai
n,
man
dibl
enu
mbn
ess,
nigh
t sw
eats
, an
d po
or
exer
cise
to
lera
nce
Not
sp
ecifi
edB
urki
tt ly
mph
oma
CT:
Nod
ular
, hom
ogen
eous
,an
d hy
pode
nse
mas
s tha
t sh
owed
min
imal
con
trast
en
hanc
emen
tM
RI:
T1 w
eigh
ted
nodu
lar,
parti
ally
wel
l-circ
umsc
ribed
,ho
mog
eneo
us, h
ypoi
nten
se
lesi
on in
the
body
of t
he
panc
reas
. T2
wei
ghte
d ho
mog
eneo
us, h
yper
inte
nse
panc
reat
ic le
sion
. Pos
t-ga
dolin
ium
T1-
wei
ghte
d,ar
eas o
f lin
ear a
nd p
unct
ate
cont
rast
enh
ance
men
t wer
e ob
serv
ed a
long
the
sept
atio
ns
insi
de th
e le
sion
.
US
guid
edfin
e ne
edle
as
pira
tion
cyto
logy
CM
TD
ied
of se
psis
af
ter 2
nd m
onth
of
chem
othe
rapy
367
PANCREATIC FOLLICULAR LYMPHOMA
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Bau
tist
et a
l.2920
09M
ale/
13
Pain
Tail
Non
-Hod
gkin
B
lym
phom
aC
T an
d M
RI s
how
ed a
wel
l de
fined
5 c
m so
lid m
ass w
ith
necr
ohae
mor
rhag
ic c
ente
r lo
cate
d in
pan
crea
s tai
l, w
ithou
t com
prom
isin
g ne
ighb
our s
truct
ures
.
CT
guid
ed b
iops
yC
MT
CR
Haj
i et a
l.3020
091
mal
e an
d 2
fem
ales
/ 52
– 65
Vagu
e ab
dom
inal
pa
in, l
ow
grad
e fe
ver,
loss
of
appe
tite
and
wei
ght,
mel
ena
(1)
Hea
d (2
), ta
il (1
)D
LBC
L (5
)C
T: H
ypod
ense
mas
s in
body
of p
ancr
eas,
head
and
ta
il (1
) enc
asin
g th
e ve
ssel
s, pe
ri-pa
ncre
atic
lym
ph n
ode
enla
rgem
ent w
ith n
o bi
le o
r pa
ncre
atic
duc
t dila
tatio
n.
CT-
guid
ed c
ore
biop
sy o
r fine
ne
edle
asp
iratio
n pr
oced
ure
(2)
CM
T+RT
(2),
PD+C
MT
(1)
CR
Sugi
shita
et
al.31
2010
Mal
e/16
A
bdom
inal
pa
in, j
aund
ice
Hea
d D
BC
LC
T: 3
.0 ×
4.5
cm
ho
mog
eneo
usly
enh
anci
ng m
ass
loca
lised
bet
wee
n th
e in
ferio
r ve
na c
ava
and
panc
reat
ic h
ead.
Th
e co
mm
on p
ancr
eatic
duc
t w
as d
ilate
d an
d th
e co
mm
on
bile
duc
t was
sten
osed
.M
RI:
Panc
reat
ic h
ead
with
lo
w si
gnal
inte
nsity
on
T1W
im
ages
and
hig
h in
tens
ity o
n T2
W im
ages
, whi
ch e
nhan
ced
inho
mog
eneo
usly
Not
don
ePD
+CM
TC
R
Abe
et a
l.3220
10M
ale/
56
Asy
mpt
o-m
atic
Hea
dB
-cel
l lym
phom
aC
T: A
5 c
m tu
mou
r loc
ated
in
the
head
of p
ancr
eas,
whi
le a
n en
hanc
ed C
T sc
an sh
owed
a
slig
ht in
crea
se in
the
tum
our
with
out e
ncas
emen
t of a
rterie
s or
vei
ns.
MR
I: Pa
ncre
atic
mas
s with
ho
mog
eneo
usly
hig
h si
gnal
in
tens
ity o
n T2
-wei
ghte
d im
ages
and
low
sign
al in
tens
ity
on T
1-w
eigh
ted
imag
es w
ith
gado
liniu
m e
nhan
cem
ent
PET/
CT:
Uni
que
inte
nse
upta
ke
of F
DG
in th
e pa
ncre
as.
Lapa
rosc
opic
as
sist
ed b
iops
yPD
-CM
TN
A
Malaysian J Pathol December 2018
368
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Ale
xand
er
et a
l.3320
11M
ale/
61
Fatig
ue,
wei
ght l
oss,
and
jaun
dice
Hea
dD
LBC
L in
as
soci
atio
n w
ith lo
w-g
rade
fo
llicu
lar
lym
phom
a in
th
e su
rrou
ndin
g ly
mph
nod
es
CT:
A 5
-cm
enh
anci
ng m
ass
that
effa
ced
the
panc
reat
ic
pare
nchy
ma
and
clos
ely
appo
sed
the
supe
rior m
esen
teric
ve
in n
ear t
he p
orta
l vei
n co
nflue
nce.
The
re w
as n
o up
stre
am d
ilata
tion
of th
e pa
ncre
atic
duc
t or i
ntra
hepa
tic
bile
duc
t. Se
vera
l bor
derli
ne to
m
ildly
enl
arge
d pe
ripan
crea
tic
and
mes
ente
ric ly
mph
nod
es
wer
e no
ted.
Fine
-nee
dle
aspi
ratio
n w
as n
ot
atte
mpt
ed d
ue to
in
terv
enin
g bl
ood
vess
els b
etw
een
the
mas
s and
the
ultra
soun
d pr
obe.
PD-C
MT
CR
And
erlo
ni
et a
l.3420
15Fe
mal
e/33
Ja
undi
ce,
feve
r, ab
dom
inal
pa
in
Hea
d N
on-H
odgk
in B
ly
mph
oma
CT:
Com
mon
bile
duc
t dila
tion
(dia
met
er 1
0 m
m) w
ith a
pa
ncre
atic
hyp
oden
se m
ass (
4.5
x 4
x 5
cm) i
nvol
ving
the
head
of
the
panc
reas
with
diff
use
enla
rged
“sa
usag
e-sh
aped
” pa
ncre
atic
gla
nd a
nd ir
regu
lar
narr
ow p
ancr
eatic
duc
t su
gges
tive
for a
utoi
mm
une
panc
reat
itis
MR
I: H
ypov
ascu
lar
enla
rgem
ent o
f the
who
le
panc
reas
with
hom
ogen
eous
en
hanc
emen
t in
the
tard
ive
phas
es a
nd m
ultip
lebi
late
ral h
ypov
ascu
lar r
enal
le
sion
s
Upp
er
gast
roin
test
inal
en
dosc
opy
(UG
IE)
guid
ed b
iops
y
CM
TC
R
Fuku
baet
al.35
2016
Fem
ale/
60
Epig
astri
c pa
in, f
ever
, w
eigh
t los
s, dr
ench
ing
nigh
t sw
eats
Hea
dD
LBC
LC
T: L
esio
n m
easu
ring
9.5
cm
in d
iam
eter
that
was
surr
ound
ed
by p
art o
f the
hep
atic
por
tal,
head
of t
he p
ancr
eas,
and
post
erio
r wal
l of d
uode
num
. Th
e m
ass h
ad a
smoo
th e
dge
and
unifo
rm d
ensi
ty, a
nd w
as o
f lo
wer
con
trast
.M
RI:
Low
inte
nsity
are
a in
T1-
wei
ghte
d im
ages
and
a sl
ight
lyhi
gh in
tens
ity a
rea
in T
2-w
eigh
ted
imag
es. T
here
wer
e no
find
ings
of n
ecro
sis o
r flui
d st
orag
e in
the
mas
s.PE
T/C
T: A
ccum
ulat
ion
of F
DG
in
the
mas
s.
Initi
al c
ytol
ogy
of
panc
reat
ic ju
ice
is
nega
tive
Endo
scop
icul
traso
und-
guid
ed
tissu
e bi
opsy
CM
TC
R
369
PANCREATIC FOLLICULAR LYMPHOMA
Aut
hors
Year
No
of C
ases
/ G
ende
r/A
geC
linic
al
pres
enta
tion
Loc
atio
n of
tu
mou
r in
pa
ncre
as
His
topa
thol
ogy
diag
nosi
sIm
agin
g fin
ding
s Pr
eope
rativ
e cy
tolo
gy/ti
ssue
bi
opsy
Trea
tmen
tO
utco
me
at im
e of
rev
iew
Lili
et a
l.3620
172
mal
es/
32-6
2Pa
in, j
aund
ice
Hea
d (1
), ta
il (1
)D
LBC
L C
T: H
eter
ogen
eous
enh
ance
d m
ass a
risin
g fr
om th
e pa
ncre
atic
hea
d an
d ta
il.
Mul
tiple
enl
arge
d ly
mph
no
des i
n th
e ab
dom
inal
ca
vity
(1)
CT
guid
ed b
iops
yPD
+ C
MT
(1)
CR
Bon
inse
gna
et a
l.3720
176
mal
es8
fem
ales
/ 41
– 8
5
Abd
omin
al
pain
or
disc
omfo
rt,
jaun
dice
, pa
lpab
le
mas
s, sy
stem
ic
sym
ptom
s
Hea
d (6
),bo
dy-ta
il (7
),w
hole
pa
ncre
as (1
)
FCL
(5),
DLB
CL
(6),
high
gra
deB
-cel
l lym
phom
a(3
)
CT:
Tum
our e
ncas
emen
t of
coe
liac
axis
, sup
erio
r m
esen
teric
arte
ry a
nd su
perio
r m
esen
teric
vei
n (5
); sp
leni
c ve
in a
nd a
rtery
enc
asem
ent
(2).
Ther
e w
ere
no si
gns o
f in
filtra
tion,
with
no
vess
el w
all
irreg
ular
ity o
r ste
nose
s. Th
ere
wer
e pr
esen
ce o
f nec
rosi
s (2)
, en
larg
ed ly
mph
nod
es (1
1),
peri-
panc
reat
ic fa
t stra
ndin
g (1
4), e
nlar
ged
com
mon
hep
atic
du
ct (6
) and
enl
arge
d m
ain
panc
reat
ic d
uct (
5).
US-
guid
ed
perc
utan
eous
bio
psy
(6),
US-
guid
ed
endo
scop
ic b
iops
y (7
), en
dosc
opic
bi
opsy
of t
he
neop
lasm
invo
lvin
g th
e du
oden
um w
all
(1)
CM
TN
A
Kon
jeti
et a
l.3820
18Fe
mal
e/68
B
elch
ing,
ab
dom
inal
bl
oatin
g,
wei
ght l
oss
Hea
dB
urki
tt ly
mph
oma
CT:
Per
ipor
tal s
olid
7.5
× 4
.9 ×
12
.7 cm
mas
s whi
ch o
bstru
cted
th
e ce
ntra
l hep
atic
duc
ts a
nd
enca
sed
the
mai
n po
rtal v
ein;
di
fficu
lt to
sepa
rate
the
lesi
on
from
live
r and
pan
crea
tic
pare
nchy
ma.
CB
D b
rush
ing
cyto
logy
sh
owed
aty
pica
l ly
mph
ocyt
es
susp
icio
us
for m
alig
nant
ly
mph
oma.
FNA
cyt
olog
y an
d tis
sue
biop
sy o
f pa
ncre
atic
hea
d
CM
TD
ied
of se
psis
and
ba
cter
iaem
ia
Abb
revi
atio
ns: A
WD
, aliv
e w
ith d
isea
se; C
BD
, com
mon
bile
duc
t; C
MT,
che
mot
hera
py; C
R, c
ompl
ete
rem
issi
on; C
T, c
ompu
ted
tom
ogra
phy;
DH
L, d
iffus
e hi
stio
cytic
lym
phom
a; D
LBC
L,
diffu
se la
rge
B c
ell l
ymph
oma;
DP,
dis
tal p
ancr
eate
ctom
y; F
NA
, fine
nee
dle
aspi
ratio
n; F
CL,
folli
cula
r cel
l lym
phom
a; L
BC
L, la
rge
B c
ell l
ymph
oma;
MR
I, m
agne
tic re
sona
nce
imag
ing;
NA
, not
av
aila
ble;
NH
BL,
non
-Hod
gkin
B ly
mph
omas
; PD
, pan
crea
ticod
uode
nect
omy;
PET
/CT,
pos
itron
em
issi
on to
mog
raph
y/co
mpu
ted
tom
ogra
phy;
PR
, par
tial r
emis
sion
; RT,
radi
othe
rapy
.
Malaysian J Pathol December 2018
370
91% of patients with pancreatic adenocarcinoma. Nonetheless the use of FNA with or without flow cytometry to diagnose lymphomas, including primary pancreatic lymphoma, has its own limitations.47 Rare cases presenting as T-cell lymphoma and Hodgkin lymphoma are often difficult to quantify on fine needle aspirate subjected to flow cytometry. Moreover, Hodgkin lymphoma often requires the identification of the characteristic Reed-Sternberg cells which may be difficult to find. In addition, the yield of endoscopic ultrasound guided FNA with flow cytometry also depends on the adequacy of material obtained during the sampling and could be missed if the endoscopist does not keep a high index of suspicion. Endoscopic ultrasound-assisted fine needle aspiration (EUS-FNA) is a valuable tool to diagnose primary pancreatic lymphoma. Flow cytometry analysis can be used as a complementary tool with conventional cytology. Pre-operative tissue biopsy or cytological diagnosis would be necessary to prevent unwarranted surgery in suspected cases involving primary pancreatic lymphoma.
CONCLUSION
It is important to differentiate between primary pancreatic lymphoma and the more common adenocarcinoma of the pancreas, as its treatment and prognosis differ significantly. Primary pancreatic lymphoma should be considered in the differential diagnosis of pancreatic tumours and an attempt to obtain preoperative tissue diagnosis such as fine needle aspiration (FNA) cytology with or without flow cytometry and/or tissue biopsy may be necessary before proceeding to radical surgery.
Conflicts of Interest: The authors declared no conflict of interest.
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