Ann Nucl Med (2013) 27:554–563
DOI 10.1007/s12149-013-0719-3

ORIGINAL ARTICLE

The usefulness of 18F-FDG PET/MRI fusion image in diagnosing
pancreatic tumor: comparison with 18F-FDG PET/CT
Shigeki Nagamachi • Ryuichi Nishii • Hideyuki Wakamatsu • Youichi Mizutani •Shogo Kiyohara • Seigo Fujita • Shigemi Futami • Tatefumi Sakae •Eiji Furukoji • Shozo Tamura • Hideo Arita • Kazuo Chijiiwa • Keiichi Kawai

Received: 19 September 2012 / Accepted: 17 March 2013 / Published online: 12 April 2013
Ó The Japanese Society of Nuclear Medicine 2013

Abstract
Purpose This study aimed at demonstrating the feasibilityof retrospectively fused 18F FDG-PET and MRI (PET/MRI
fusion image) in diagnosing pancreatic tumor, in particulardifferentiating malignant tumor from benign lesions. In
addition, we evaluated additional findings characterizing
pancreatic lesions by FDG-PET/MRI fusion image.
Methods We analyzed retrospectively 119 patients: 96
cancers and 23 benign lesions. FDG-PET/MRI fusion
images (PET/T1 WI or PET/T2WI) were made by dedicated software using 1.5 Tesla (T) MRI image and FDGPET images. These images were interpreted by two welltrained radiologists without knowledge of clinical information and compared with FDG-PET/CT images. We
compared the differential diagnostic capability between
PET/CT and FDG-PET/MRI fusion image. In addition, we
evaluated additional findings such as tumor structure andtumor invasion.
Results FDG-PET/MRI fusion image significantly
improved accuracy compared with that of PET/CT (96.6

vs. 86.6 %). As additional finding, dilatation of main
pancreatic duct was noted in 65.9 % of solid types and in
22.6 % of cystic types, on PET/MRI-T2 fusion image.
Similarly, encasement of adjacent vessels was noted in
43.1 % of solid types and in 6.5 % of cystic types. Particularly in cystic types, intra-tumor structures such as
mural nodule (35.4 %) or intra-cystic septum (74.2 %)were detected additionally. Besides, PET/MRI-T2 fusion
image could detect extra benign cystic lesions (9.1 % in
solid type and 9.7 % in cystic type) that were not noted by
PET/CT.
Conclusions In diagnosing pancreatic lesions, FDG-PET/MRI fusion image was useful in differentiating pancreaticcancer from benign lesions. Furthermore, it was helpful inevaluating relationship between lesions and surrounding
tissues as well as in detecting extra benign cysts.
Keywords 18F FDG-PET/CT  18F FDG-PET/MRI fusion
image  Pancreatic tumor

Introduction
S. Nagamachi (&)  R. Nishii  H. Wakamatsu  Y. Mizutani 
S. Kiyohara  S. Fujita  S. Futami  T. Sakae  E. Furukoji 
S. Tamura  H. Arita
Department of Radiology, School of Medicine, Miyazaki
University, 5200 Kihara, Kiyotake, Miyazaki-city,
Miyazaki Prefecture 889-1692, Japane-mail: snagama@med.miyazaki-u.ac.jp
K. Chijiiwa
Department of the 1st Surgery, Faculty of Medicine,
Miyazaki University, 5200 Kihara, Kiyotake, Miyazaki-city,
Miyazaki Prefecture 889-1692, JapanK. Kawai
Faculty of Health Science, School of Medicine, Kanazawa
University, Kanazawa, Ishikawa Prefecture 920-8640, Japan

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F-fluorodeoxyglucose (FDG)-positron emission tomography (PET)/CT is helpful in staging of pancreatic cancer[1–3]. As for differential diagnosis, it is difficult to distinguish pancreatic cancer from various benign lesions offocal FDG uptake such as inflammatory lesion [4]. Standardized uptake value (SUV) of FDG-PET is a ordinary
used quantitative index for diagnosing pancreatic cancer.
The dual time point evaluation is one of methods for
improving diagnostic ability [5, 6]. Still some overlaps
exist between malignancy and benign lesions, for example,
pancreatic cancer of relatively low SUV values or pancreatitis of high SUV value [7–9]. Therefore, it is difficult

Ann Nucl Med (2013) 27:554–563

setting optimal SUV cut-off level to differentiate malignancy from benign lesions.
In this regard, 18F-FDG-PET/CT allows precise coregistration of metabolically active lesions and anatomical
abnormalities, and it can make up for a drawback of PET[10, 11]. However, the accuracy of 18F-FDG-PET/CT without
contrast media in assessing structures of cystic lesion such as
intraductal papillary mucinous neoplasm (IPNM) remains
inadequate. In addition, diagnosis of local involvement suchas main pancreatic duct (MPD) invasion or peri-pancreatic
nodal involvement remains inadequate, either. One of reasons for poor performance of FDG-PET/low-dose CT in
diagnosing pancreatic lesion is insufficiency in visualizing
anatomic border of similar density. Although the breath-holdtechnique can improve the tumor delineation and also thequantification of SUV measurements [12], it is not always
available in the patients with respiratory failure.
MRI is suitable for evaluating boundary between pancreas and surrounding tissues because of its superiority intissue contrast resolution. Indirect findings associated withcancer invasion, such as pancreatic duct dilatation or collateral veins dilatation, will also be evaluable. In addition,
qualitative diagnoses such as necrosis, cystic degenerationor fibrotic changes are possible using MRI [13]. Integrated
MR/PET scanners have recently been developed andexpected to perform as a new powerful multimodality
imaging tool [14–16]. An improved soft tissue contrast
provided by MR created different image sets, which may
establish better diagnostic tree in various field. However,owing to limited availability of hybrid PET/MRI system,
PET/MR fusion images using software are still now used invarious lesions [17–20]. Recently, Tatsumi et al. reported
that PET/MRI fusion, especially PET with T1WI, is superior to PET/CT in characterizing pancreatic tumors [20].
However, the former study did not address the usefulness inthe differential diagnosis of cystic lesion such as benign
IPMN or intraductal papillary mucinous carcinoma (IPMC).
The current study was done to investigate the feasibilityof utilizing 18F-FDG PET/MRI fusion images to differentially diagnose pancreatic cancer from benign lesions bydividing into solid lesions and cystic lesions. In addition, we
evaluated the diagnosability of cancer invasion into pancreatic duct or surrounding structures. Also, we evaluatedthe diagnosability of detecting further additional lesions.

Materials and methods
Patients
One-hundred and nineteen patients (64 males, 55 females;
average age 67.1 years; range 34–85 years) with cytologyproven or biopsy-proven diagnosis of pancreatic lesion

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Table 1 Clinicopathological profiles of patients (n = 119)
Mean ± SD (range) or n (%)
Age (years)

67.0 ± 10.5 (34–85)

Gender (M:F)

64:55

Location of lesions
Head

66 (55.4)

Body

37 (31.1)

Tail

16 (13.4)

Maximum tumor diameter (cm)

3.6 ± 1.8 (1.1–12.0)

SUVmax (early)

7.1 ± 3.8 (2.3–23.9)

SUVmax (delayed)

8.8 ± 4.7 (2.5–28.5)

Table 2 Tumor characteristics (n = 119)
Diagnosis

S:C

Malignancy
Invasive ductal carcinoma

75 (71:4)

Intraductal papillary-mucinous carcinoma

12 (0:12)

Mucinous cyst-adenocarcinoma

6 (0:6)

Malignant endocrine tumor

3 (3:0)

BenignPancreatitis

14 (14:0)

Intraductal papillary-mucinous neoplasm

6 (0:6)

Serous cyst adenoma

3 (0:3)119 (88:31)

S solid type, C cystic typewere included (Tables 1, 2). The diseases comprised of 75
invasive ductal carcinoma, 12 intraductal papillary-mucinous
carcinoma (IPMC), 6 mucinous cyst-adenocarcinoma, 3malignant endocrine tumor, and 23 benign lesions (14chronic pancreatitis, 6 benign intraductal papillary mucinous
neoplasm (IPMN) and 3 serous cyst-adenoma). In 75 cases ofinvasive ductal carcinoma, 4 cases were cystic type invasive
carcinoma derived from intraductal tumor. Although 8 cases
were clinically diagnosed as un-resectable advanced invasive
ductal carcinoma based on the preoperative image findings.
In 14 cases of chronic pancreatitis, 10 cases were finallydiagnosed as mass-forming pancreatitis. Although etiology ofother 4 cases was unknown, they were diagnosed as pancreatitis during course observation.
Among cancer patients, 20 cancers were diagnosed to be
un-resectable, and 76 patients eventually underwent surgery
with a curative intention, although the cancer turned out to be
un-resectable in 8 because of intra-operative findings. As forstaging by UICC, they were categorized as stage I 13, stage
IIA 12, stage IIB 14, stage III 18, and stage IV 39.
Patients fasted for at least 5 h. The blood glucose level,measured just before tracer administration, was \140 mg/dl
in all patients. Although 12 patients had diabetes, the controlof blood glucose was relatively maintained by drug therapy.

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Data acquisition and image reconstruction

Image interpretation

We performed FDG-PET/CT study using a whole-body
PET/CT system (Biograph 16; Siemens/CTI, Knoxville,TN). The CT component of PET/CT corresponds to a
16-slice multi-detector-row spiral CT scanner (sensation
16; Siemens) with a transverse FOV of 500 mm and a
spatial resolution greater than 1 mm. The PET componentof PET/CT allowing 3-dimensional-only acquisition with afield of view (FOV) of 700 mm in the trans-axial direction
and 170 mm in the axial direction. The intrinsic resolution
is 4.2 mm full width at half maximum. Whole-body FDGPET/CT images were obtained using the three-dimensional
method 60 min after injection of 185–220 MBq FDG. The
images were obtained from the top of the brain to the femur
in all patients. We did not use intravenous contrast media.
Low-dose plain CT (40 mAs) images were used for anatomical localization. CT-based attenuation correction used
700-mm extended FOV technology (Auto AC; Siemens). All
PET images were reconstructed using iterative algorithms(Fourier rebinning plus attenuation-weighted ordered-subset
expectation maximization, 4 iterations, 8 subset, 5-mm
Gaussian filter) with CT-based attenuation correction. The
data were reconstructed with a 256 9 256 matrix and 3-mm
slice thickness. All PET and CT images were transferred to a
dedicated workstation (ESOFT4.5, Siemens), from which
fused PET/CT images were constructed.
We used the following protocol: all patients fasted for atleast 5 h before injection of 185 MBq of 18F-FDG. During
the uptake phase of approximately 50 min, the patientsremained in a quiet position. The first whole body image
was done in a supine position. The imaging time was
15–18 min for each patient. In addition to the conventional
PET/CT examination, we added an abdominal imaging of aspot view 30 min after the end of the first whole body
imaging.
MRI was performed with either 1.5 T scanner (VANTAGE, Toshiba). As the CT portion of PET/CT was performed without contrast media, non-CE transaxial T1- andT2-weighted images (WI) were used for comparison andfor fusion with FDGPET. The following were the imaging
parameters: In T1 WI, TR 140 ms, TE 2.4 or 4.8 ms, flip
angle 70, 6.0 mm slice thickness/1 mm inter-slice gap. In
T2WI, TR 3300 ms, TE 90 ms, flip angle 90, 6.0 mm slice
thickness/1 mm inter-slice gap.
Both T1WI and T2WI covering pancreatic lesions werefused with PET image automatically using a dedicatedsoftware (Fusion 7D, DX MM FOR WINDOWS. VER.6.1.4,
MEDASYS JAPAN). Morphological information including
the size and internal structure (cystic or solid) was recorded.
All patients provided written informed consent. This
study protocol was approved by the review board of theinstitution.

Image interpretations were performed on a dedicatedworkstation (ESOFT4.5, Siemens), which can display threeorthogonal planes for CT, PET, and PET/CT fusion images(sagittal, coronal, and trans-axial) and maximum-intensityprojection (MIP) images. These images were visuallyassessed for accuracy of fusion and alignment in separate
instances by the same nuclear medicine radiologists, whowere unaware of the clinical information.
The diagnosis by PET/CT was done by two experienced
nuclear medicine specialists according to the following
criterion: namely, the lesion was diagnosed as malignant
when the localized FDG uptake higher than surrounding
normal pancreatic tissue was visually observed [20]. Even
if the degree of FDG uptake was faint on the early image, it
was defined as malignant when FDG uptake increased on
the delayed image. It was defined as benign when there was
no apparent FDG uptake, and was considered as chronicpancreatitis when localized FDG uptake was noted in
multiple calcifications [21]. Decisions on the findings werereached by consensus.
Each PET/MRI fusion image was interpreted by two
well-trained radiologists without knowledge of clinicalinformation. The diagnosis of pancreatic cancer wasdetermined when following findings were noted on PET/MRI fusion images: namely, there were irregular shaped
solid mass with or without FDG uptake. In cystic tumor,
existence of FDG uptake component was diagnosed as
malignancy. In addition, existence of mural nodule matched criteria with or without FDG uptake. Even if there
was FDG uptake, we diagnosed it as benign when we could
not detect any apparent mass or following indirect findings
indicating malignancy. Namely, abrupt interruption of
main pancreatic duct (MPD) due to tumor accompanying
smooth dilation of tail side duct was considered as positive
finding [22]. In contrast, multifocal strictures and dilatations of MPD and dilatation of the side-branches, so called‘beaded appearance’, were considered to be findings suggestive of chronic pancreatitis [23].
As for invasion to surrounding vasculatures, it wasdiagnosed by following findings: (1) encasement or occlusion of vessel, with or without collaterals (2) infiltration oftumors to peri-vascular fat tissue (3) circumferential contact
of more than 180° between the tumor and the vessel, and (4)mass effect along one side of the vessel for more than 2 cm
[24–27]. Invasion on CBD was diagnosed by the dilatationof CBD [28, 29]. Similarly, invasion to adjacent GI tract
was diagnosed by the finding indicating broad contact totumor with irregularity of GI tract contour [29].
Finally, the image findings were carefully correlated tosurgical and pathologic records. Then, following issues
were evaluated: (1) comparison of diagnostic capabilities

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557

between PET/CT and PET/MRI fusion image (Differential
diagnosis of primary lesion). Diagnostic capabilities
included sensitivity (Sen), specificity (Spe), positive-predictive value (PPV), negative-predictive value (NPV), andaccuracy (ACC). Regarding PET/MRI fusion images, weconsidered the diagnosis correct if either PET/MRI-T1WIor PET/MRI-T2WI diagnosed them correctly. (2) Comparison of the frequency of additional information, such as
intra-tumor structure, relationship between tumor and surrounding tissues and additional lesions, among PET/CT,
PET/MRI-T1W I, and PET/MRI-T2WI.
All subjects were divided into solid lesions and cystic
lesions and were evaluated, respectively, regarding above
issues. Based on intra-operative and pathological findings, thedetectability of cancer invasions to GI tract, CBD, and vessels
were compared between PET/CT and PET/MRI fusion images.

Table 3 Comparison of diagnostic capability between PET/CT and
PET/MRI fused image (differential diagnosis)
Sens.

Spec.

PPV

NPV

Acc.

PET/CT (total) (n = 119)

96.9

43.5

87.7

76.9

86.6

PET/MRI (total)(n = 119)99.0

82.6***

96.9

95.2

96.6*

PET/CT (solid) (n = 88)
PET/MRI (solid) (n = 88)

97.4
98.7

21.4
92.9

86.7
98.7*

60.0
92.9

85.2
97.7**PET/CT (cystic) (n = 31)

95.5

77.8

91.3

87.5

90.3

PET/MRI (cystic)(n = 31)

100.0

77.8

91.7

100.0

93.5

Results are expressed in %* P = 0.005, ** P = 0.004, *** P = 0.003
P = 0.003,

P = 0.002

Statistical analysis
Methods were compared on a per-lesion basis. Diagnostic
characteristics (Sens., Spec., PPV, NPV and Acc), wereanalyzed using the McNemar test (Sen, Spe, ACC) and Chi
square test (PPV, NPV). A P value of less than 0.05 wasconsidered to be a statistically significant difference. Statistical analyses were performed with statistical software
Stat Flex (Version 6.0, Artech, Osaka, Japan).

Results
In comparing diagnostic capabilities between PET/CT and
PET/MRI fusion images, the latter demonstrated significant
better Acc (86.6 vs. 96.6 %). Similarly, both Spec. and
PPV significantly improved (43.5 vs. 82.6 % and 87.7 vs.
96.9 %) (Table 3). Twelve of 119 cases (10.0 %) werediagnosed correctly based only on morphological diagnosis
by PET/MRI fusion images.
In the analysis of solid type tumor, Acc was significantly
better in PET/MRI fusion images compared with that of
PET/CT images (85.2 vs. 97.7 %). Spec. and PPV of PET/MRI fusion images also improved significantly comparedwith those of PET/CT images (21.4 vs. 92.9 %, 86.7 vs.
98.7 %). As for the cystic lesion, there was no statisticalsignificance between PET/MRI fusion image and PET/CT.
As additional findings, intra-tumor structure such as internal septum (74.2 %) or mural nodule (35.4 %) was frequently
noted on PET/MRI-T2 fusion image (Table 4). In particular,presence of mural nodule was diagnostic finding suggesting
malignancy with or without uptake of FDG (Figs. 1, 2). Multilocular structure was also often recognized by PET/MRI-T2

Table 4 Additional findings
detected by PET/CT and PET/MRI fusion images(T1) PET/MRI-T1 fusion image,(T2) PET/MRI-T2 fusion image,
MPD main pancreatic duct,
CBD common bile duct, GI
gastro-intestinal

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Fig. 1 Low-dose CT showed cystic lesion of pancreas tail (leftupper). FDG-positive lesion was noted in the cystic tumor by PET/CT(left lower). Mural nodule was noted on MRI T1WI (center upper).
Accordant FDG uptake with mural nodule was noted on PET/MRI-T1

fusion image (center lower). Mural nodule in cystic tumor was notedon MRI-T2WI (right upper) and FDG uptake accordant with mural
nodule was clearly noted by PET/MRI-T2 fusion image (right lower).
These findings suggested IPMC, which was pathologically provenFig. 2 Low-dose CT (left lower) and PET/CT (left upper) demonstrated FDG-negative cystic lesion adjacent to duodenum. The casewas diagnosed as IPMN by PET/CT. PET/MRI-T1 fusion image
showed intra cystic septum without FDG uptake (right upper). PET/MRI-T2 fusion image demonstrated FDG-negative mural nodule inthe multilocular cystic lesion (white arrow), which was suggested to
be an intra-ductal papillary mucinous carcinoma (IPMC). The
diagnosis was confirmed by surgical operation (right lower)

fusion image, and the localized FDG uptake within multilocular structure was confirmed to be malignancy.
Cancer invasion to surrounding vessel, CBD, gastrointestinal tract, or MPD were also detected by PET/MRI fusion
image: particularly, MPD obstruction by cancer invasion anddilatation of upper stream were clearly visualized with PET/MRI-T2WI [30] (Fig. 3). In chronic pancreatitis, irregular
contour of pancreatic duct is frequently shown. As noted in
representative case, MPD showed beaded dilatation andirregularity of ductal contour (Fig. 4). The case was diagnosed as autoimmune pancreatitis during course observation.
As for relationship between the tumor and adjacent vessels

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559

Fig. 3 Although low dose CT did not show any abnormal density
area (left upper), PET/CT showed intense uptake in accord withpancreatic head cancer (left lower). Both PET/MRI-TIWI fusion

image (right upper) and PET/MRI-T2WI fusion image (right lower)
demonstrated dilation of MPD (black arrow), but PET/MRI-T2WI
showed more understandable image

Fig. 4 Low-dose CT showed localized swelling of pancreatic body(left upper). Intense FDG uptake was noted in pancreatic body by
PET/CT (left lower) and the case was considered as pancreas cancer.
PET/MRI-T1WI fusion image showed similar information (rightupper). PET/MRI-T2WI fusion image showed beaded dilatation of
pancreatic duct (white arrow), which suggested chronic inflammatorychange (right lower). The case was diagnosed as autoimmune
pancreatitis during observation period

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Fig. 5 Although FDG-positive
uptake accordant with invasive
ductal carcinoma was noted, therelationship with vessel was
unclear on PET/CT (left upper,
left lower). In contrast PET/MRI-T2WI (right upper, rightlower) showed that splenicartery was interrupted by FDG
uptake tumor, which suggested
vascular invasion (white arrow).
The vessel invasion was
pathologically confirmed

like splenic artery, encasement was visualized better by PET/MRI fusion image (Fig. 5). As an additional finding, PET/MRI fusion image could detect additional complicated cysts
in almost 10 % in both solid lesion and cystic lesion.
The detectability of invasion was significantly higher in
PET/MRI compared with PET/CT, vessels (61.2 vs.
13.4 %), CBD (54.1 vs. 10.8 %), and GI tract (29.8 vs.
10.6 %) respectively (Table 5).

Discussion
The current study demonstrated that PET/MRI fusion
image gave better diagnostic performance compared withthat of FDG-PET/CT in the differentiation of pancreaticcancer. Twelve of 119 cases (10.0 %) were accurately
diagnosed based only on morphological diagnosis by PET/
MRI.
Diagnosing solid type pancreatic cancer becomes easy
when typical finding like irregular shaped low-density mass
is noted on computed tomography (CT) [31]. However, indiagnosing CT without contrast-media, cancer is easily
overlooked if tumor has the similar density like normal
pancreatic tissue [22]. In such cases, high FDG uptake inaccordance with mass lesion is the diagnostic finding suggesting pancreatic cancer [1, 6, 7, 9, 10, 32]. However,inflammatory cells also show increased FDG uptake
because of accelerated glucose metabolism; therefore, thedifferential diagnosis between active pancreatitis and cancer is difficult [1]. In general, FDG uptake pattern was often
noted as diffuse uptake in AIP [4]. Nevertheless, when AIP
appeared as focal mass persistently it can be mistaken for123

pancreatic cancer [9, 11, 33]. Although the diagnostic
sensitivity of PET/CT in solid lesion was superior to previous report [10], its accuracy was not so good because we
could not differentiate non-calcified chronic pancreatitis
from pancreatic cancer. In this respect, indirect diagnostic
valuable findings were helpfully added by PET/MRI fusion
image. Particularly, finding of main pancreatic duct (MPD),
such as dilation of caudal side when cancer invades MPD,
was useful information [34]. Although there are some
exceptions [35], it is a reliable diagnostic finding for differential diagnosis [30]. In chronic pancreatitis, moderately
tortuous dilatation and irregularity of MPD, so called
Beads-forming dilatation of MPD, is noted [34]. However,even if spindly contour or disruption of MPD is seen, no
dilatation of upstream side is noted [34]. In the current
study, PET/MRI fusion images provided diagnostic findingssuch as non-dilated MPD within high FDG uptake of pancreatic mass, which suggested mass-forming pancreatitis. In
addition, beaded dilation of MPD which was not precisely
shown by low-dose plain CT was also visualized clearly by
PET/MRI fusion images. Diffuse enlargement of the pancreas and effacement of the lobular contour of the pancreas,
the so-called ‘‘sausage-like’’ appearance, a typical findingof AIP [36, 37], was also more clearly depicted by PET/MRI fusion images. Thus diagnostic accuracy was
improved significantly in solid lesions.
Both18F-FDG-PET and18F-FDG-PET/CT are useful fordifferential diagnosis in various cystic pancreas tumor [2,9, 38, 39]. Among these tumors, the correct diagnosis of
IPNM is very important because it is a slow-growing tumor
with hyperplasia-adenoma-carcinoma sequence pathologically [40]. Multilocular cystic mass with large tumor

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Table 5 Comparison of detectability of peri-pancreatic invasion
by PET/CT and PET/MRI fusion images pancreas cancer

CBD common bile duct, GI gastro-intestinal* P \ 0.01

diameter and intense FDG uptake can be easily diagnosed
as malignant cystic tumor [38]. However, there are someoverlaps of FDG uptake between benign cystic lesions andmalignant cystic tumors [2]. In this respect, MRI is beneficial in diagnosing cystic mass precisely by visualizing
solid component such as mural nodule or capsule structure[34, 41–44]. We could demonstrate both multi-locular
structures and mural nodule clearly by fusion PET/MRI-T2
images in the current study. However, the statistical significance was not noted between PET/CT and PET/MRI
fusion images in the current study. The possible reason wasthat few malignant cystic tumor cases had FDG-negative
intramural nodule. In addition, no patients of false-positive
cases such as inflammatory cystic lesions were included,
either. We should recheck the statistical significance byanalyzing more patients with cystic lesions having mural
nodule.
It is extremely important to diagnose cancer invasion of
peri-pancreatic tissues. The most important preoperative
factor for resectability is vascular invasion into superior
mesenteric artery (SMA) or celiac artery [24], which isvery difficult to determine using FDG-PET [45]. In general,
vascular invasions are diagnosed based on extensive circumferential contact between cancer and vessels, occlusionof vessels, or the mass effect of one side of the vessel[24–26]. Low-dose CT can evaluate vessels, but it is sometimes
unfeasible owing to limited density resolution. In contrast, MRI
has an excellent diagnostic ability to detect vascular invasion[24]. In the current study, encasements of major vessels such as
gastro-colic trunk or splenic vein were better visualized with
PET/MRI-T2 fusion images in about the half of solid typecancers, which suggested unresectability or altered surgicalstrategy.
Although reliable imaging method for diagnosing cancer
invasion into extra-pancreatic nerve plexus (PLX) has notbeen established, it is one of the important issues in choosing
treatment strategy and predicting prognosis [46, 47]. Streaky
and strand-like signal intensity structures in fat tissue, using
MRI, have been used to diagnose PLX invasion [46]. In thecurrent study, some of the advanced pancreatic cancer cases

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showed streak-like structure with intense FDG uptake suggesting PLX invasion, but it was not confirmed surgically.
Future analyses with larger numbers of patients need to be
conducted in resolving the problem.
As an additional finding, cystic lesions such as pseudocyst or retention cyst due to obstruction of MPD are
sometimes found in pancreas cancer or pancreatitis[42, 48]. In the current study, PET/MRI-T2 fusion image
detected them unexpectedly in about 10 % of cases.
The current study has some limitations. First, fusionimages were made retrospectively by paired images taken
at a few days’ intervals. Therefore, misregistration of PET
and MRI image due to dislocation of organs between two
examinations was unavoidable.
The second limitation was that used T1WI for the fusion
was without fat-suppression. Because fat-suppression T1WI
can delineate contour of pancreas better, FDG-PET/fat-suppression T1W fusion image may have accomplished better
diagnosability in evaluating vascular encasement or CBD
invasion. In our retrospective analyses, we used T1WI
without fat-suppression for PET/MRI fusion because some of
the current cases did not choose fat-suppression T1. This
limitation caused disadvantageous results to PET/T1 MRI
fusion images compared with PET/MRI T2 images inassessing peri-pancreatic invasion. Future studies should be
evaluated with FDG-PET/fat-suppression T1WI MRI fusion.

Conclusion
Regarding pancreatic tumor, FDG-PET/MRI fusion image
proved to be useful in differentiating pancreatic cancerfrom benign lesion although the statistically significant
difference was confirmed only in solid lesions.
In addition, the relationship with the surrounding orinternal structures such as blood vessels, bile duct system,and pancreatic duct became more apparent, thus helping
evaluate cancer invasion and detect other benign cystic
lesions as well.

References
1. Murakami K. FDG-PET for hepatobiliary and pancreatic cancer:
advances and current limitations. World J Clin Oncol.
2011;2:229–36.
2. Takanami K, Hiraide T, Tsuda M, Nakamura Y, Kaneta T,
Takase K, et al. Additional value of FDG PET/CT to contrastenhanced CT in the differentiation between benign and malignant
intraductal papillary mucinous neoplasms of the pancreas withmural nodules. Ann Nucl Med. 2011;25:501–10.
3. Berberat P, Friess H, Kashiwagi M, Beger HG, Buchler MW.
Diagnosis and staging of pancreatic cancer by positron emission
tomography. World J Surg. 1999;23:882–7.

123

562
4. Nakamoto Y, Saga T, Ishimori T, Higashi T, Mamede M, Okazaki K, et al. FDG-PET of autoimmune-related pancreatitis:
preliminary results. Eur J Nucl Med. 2000;27:1835–8.
5. Okano K, Kakinoki K, Akamoto S, Hagiike M, Usuki H, Yamamoto Y, et al. 18F-fluorodeoxyglucose positron emission
tomography in the diagnosis of small pancreatic cancer. World J
Gastroenterol. 2011;17:231–5.
6. Lyshchik A, Higashi T, Nakamoto Y, Fujimoto K, Doi R,
Imamura M, et al. Dual-phase 18F-fluoro-2-deoxy-D-glucose
positron emission tomography as a prognostic parameter inpatients with pancreatic cancer. Eur J Nucl Med Mol Imaging.
2005;32:389–97.
7. Friess H, Langhans J, Ebert M, Beger HG, Stollfuss J, Reske SN,
et al. Diagnosis of pancreatic cancer by 2[18F]-fluoro-2-deoxy-Dglucose positron emission tomography. Gut. 1995;36:771–7.
8. Stollfuss JC, Glatting G, Friess H, Kocher F, Berger HG, Reske
SN. 2-(fluorine-18)-fluoro-2-deoxy-D-glucose PET in detection of
pancreatic cancer: value of quantitative image interpretation.
Radiology. 1995;195:339–44.
9. Higashi T, Saga T, Nakamoto Y, Ishimori T, Fujimoto K, Doi R,
et al. Diagnosis of pancreatic cancer using fluorine-18 fluorodeoxyglucose positron emission tomography (FDG PET)—usefulness and limitations in ‘‘clinical reality’’. Ann Nucl Med. 2003;
17:261–79.
10. Schick V, Franzius C, Beyna T, Oei ML, Schnekenburger J,
Weckesser M, et al. Diagnostic impact of 18F-FDG PET-CT
evaluating solid pancreatic lesions versus endosonography,
endoscopic retrograde cholangio-pancreatography with intraductal ultrasonography and abdominal ultrasound. Eur J Nucl
Med Mol Imaging. 2008;35:1775–85.
11. Nguyen VX, Nguyen CC, Nguyen BD. (18)F-FDG PET/CT
imaging of the pancreas: spectrum of diseases. J Pancreas 2011;
12:557–66.
12. Nagamachi S, Wakamatsu H, Kiyohara S, Fujita S, Futami S,
Arita H, et al. Usefulness of a deep-inspiration breath-hold 18FFDG PET/CT technique in diagnosing liver, bile duct, and pancreas tumors. Nucl Med Commun. 2009;30:326–32.
13. Mergo PJ, Helmberger TK, Buetow PC, Helmberger RC, Ros PR.
Pancreatic neoplasms: mR imaging and pathologic correlation.
Radiographics. 1997;17:281–301.
14. Schlemmer HP, Pichler BJ, Krieg R, Heiss WD. An integrated
MR/PET system: prospective applications. Abdom Imaging.
2009;34:668–74.
15. Schwenzer NF, Schraml C, Muller M, Brendle C, Sauter A,
Spengler W, et al.: Pulmonary lesion assessment: comparison ofwhole-body hybrid MR/PET and PET/CT imaging—pilot study.
Radiology. 2012;264:551–8.
16. Drzezga A, Souvatzoglou M, Eiber M, Beer AJ, Furst S, Martinez-Moller A, et al. first clinical experience with integrated
whole-body PET/MR: comparison to PET/CT in patients with
oncologic diagnoses. J Nucl Med. 2012;53:845–55.
17. Donati OF, Hany TF, Reiner CS, von Schulthess GK, Marincek
B, Seifert B, et al. Value of retrospective fusion of PET and MR
images in detection of hepatic metastases: comparison with 18FFDG PET/CT and Gd-EOB-DTPA-enhanced MRI. J Nucl Med.
2010;51:692–9.
18. Nakajo K, Tatsumi M, Inoue A, Isohashi K, Higuchi I, Kato H,
et al. Diagnostic performance of fluorodeoxyglucose positronemission tomography/magnetic resonance imaging fusion imagesof gynecological malignant tumors: comparison with positronemission tomography/computed tomography. Jpn J Radiol.
2010;28:95–100.
19. Ruf J. Lopez Hanninen E, Bohmig M, Koch I, Denecke T, Plotkin
M, et al.: Impact of FDG-PET/MRI image fusion on the detectionof pancreatic cancer. Pancreatology. 2006;6:512–9.

123

Ann Nucl Med (2013) 27:554–563
20. Tatsumi M, Isohashi K, Onishi H, Hori M, Kim T, Higuchi I, et al.
18F-FDG PET/MRI fusion in characterizing pancreatic tumors:comparison to PET/CT. Int J Clin Oncol. 2011;16:408–15.
21. Miller FH, Keppke AL, Wadhwa A, Ly JN, Dalal K, Kamler VA.
MRI of pancreatitis and its complications: part 2, chronic pancreatitis. Am J Roentgenol. 2004;183:1645–52.
22. Ros PR, Mortele KJ. Imaging features of pancreatic neoplasms.
JBR-BTR. 2001;84:239–49.
23. Vitellas KM, Keogan MT, Spritzer CE, Nelson RC. MR cholangiopancreatography of bile and pancreatic duct abnormalities
with emphasis on the single-shot fast spin-echo technique.
Radiographics. 2000;20:939–57.
24. Buchs NC, Chilcott M, Poletti PA, Buhler LH, Morel P. Vascularinvasion in pancreatic cancer: imaging modalities, preoperative
diagnosis and surgical management. World J Gastroenterol.
2010;16:818–31.
25. Lu DS, Reber HA, Krasny RM, Kadell BM, Sayre J. Local
staging of pancreatic cancer: criteria for unresectability of major
vessels as revealed by pancreatic-phase, thin-section helical CT.
Am J Roentgenol. 1997;168:1439–43.
26. Nakayama Y, Yamashita Y, Kadota M, Takahashi M, Kanemitsu
K, Hiraoka T, et al. Vascular encasement by pancreatic cancer:
correlation of CT findings with surgical and pathologic results.
J Comput Assist Tomogr. 2001;25:337–42.
27. Li H, Zeng MS, Zhou KR, Jin DY, Lou WH. Pancreatic adenocarcinoma: the different CT criteria for peripancreatic majorarterial and venous invasion. J Comput Assist Tomogr. 2005;29:
170–5.
28. Arakawa A, Yamashita Y, Namimoto T, Tang Y, Tsuruta J,
Kanemitsu K, et al. Intraductal papillary tumors of the pancreas.
Histopathologic correlation of MR cholangiopancreatography
findings. Acta Radiol. 2000;41:343–7.
29. Lopez HE, Amthauer H, Hosten N, Ricke J, Bohmig M, Langrehr
J, et al. Prospective evaluation of pancreatic tumors: accuracy of
MR imaging with MR cholangiopancreatography and MR angiography. Radiology. 2002;224:34–41.
30. Irie H, Honda H, Aibe H, Kuroiwa T, Yoshimitsu K, Shinozaki
K, et al. MR cholangiopancreatographic differentiation of benign
and malignant intraductal mucin-producing tumors of the pancreas. AJR Am J Roentgenol. 2000;174:1403–8.
31. Ardengh JC, Goldman SM, de Lima-Filho ER. Current role ofimaging methods in the diagnosis of cystic solid pancreas neoplasms: part II. Rev Col Bras Cir. 2011;38:192–7.
32. Zimny M, Schumpelick V. Fluorodeoxyglucose positron emission tomography (FDG-PET) in the differential diagnosis ofpancreatic lesions. Chirurg. 2001;72:989–94.
33. Sahani DV, Sainani NI, Deshpande V, Shaikh MS, Frinkelberg
DL. Fernandez-del Castillo C: Autoimmune pancreatitis: disease
evolution, staging, response assessment, and CT features that predict
response to corticosteroid therapy. Radiology. 2009;250:118–29.
34. Hakime A, Giraud M, Vullierme MP, Vilgrain V. MR imaging of
the pancreas. J Radiol. 2007;88:11–25.
35. Sugiyama M, Izumisato Y, Abe N, Masaki T, Mori T, Atomi Y.
Pancreatic carcinoma that completely obstructs the Wirsung duct
without dilatation of the main pancreatic duct. J Gastroenterol
Hepatol. 2006;21:1154–6.
36. Takuma K, Kamisawa T, Gopalakrishna R, Hara S, Tabata T,
Inaba Y, et al. Strategy to differentiate autoimmune pancreatitis
from pancreas cancer. World J Gastroenterol. 2012;18:1015–20.
37. Sahani DV, Kalva SP, Farrell J, Maher MM, Saini S, Mueller PR,
et al. Autoimmune pancreatitis: imaging features. Radiology.
2004;233:345–52.
38. Fischer MA, Donati O, Heinrich S, Weber A, Hany TF, Soldini
D, et al. Intraductal oncocytic papillary neoplasm of the pancreas:a radio-pathological case study. J Pancreas. 2010;11:49–54.

Ann Nucl Med (2013) 27:554–563
39. Sperti C, Pasquali C, Chierichetti F, Liessi G, Ferlin G, Pedrazzoli S. Value of 18-fluorodeoxyglucose positron emission
tomography in the management of patients with cystic tumors of
the pancreas. Ann Surg. 2001;234:675–80.
40. Baiocchi GL, Portolani N, Bertagna F, Gheza F, Pizzocaro C,
Giubbini R, et al. Possible additional value of 18FDG-PET inmanaging pancreas intraductal papillary mucinous neoplasms:
preliminary results. J Exp Clin Cancer Res. 2008;27:10.
41. Ku YM, Shin SS, Lee CH, Semelka RC. Magnetic resonanceimaging of cystic and endocrine pancreatic neoplasms. Top Magn
Reson Imaging. 2009;20:11–8.
42. Kalb B, Sarmiento JM, Kooby DA, Adsay NV, Martin DR. MR
imaging of cystic lesions of the pancreas. Radiographics.
2009;29:1749–65.
43. Pilleul F, Rochette A, Partensky C, Scoazec JY, Bernard P,
Valette PJ. Preoperative evaluation of intraductal papillary
mucinous tumors performed by pancreatic magnetic resonanceimaging and correlated with surgical and histopathologic findings. J Magn Reson Imaging. 2005;21:237–44.

563
44. Schima W. MRI of the pancreas: tumours and tumour-simulatingprocesses. Cancer Imaging. 2006;6:199–203.
45. Izuishi K, Yamamoto Y, Sano T, Takebayashi R, Masaki T,
Suzuki Y. Impact of 18-fluorodeoxyglucose positron emission
tomography on the management of pancreatic cancer. J Gastrointest Surg. 2010;14:1151–8.
46. Zhang XM, Mitchell DG, Witkiewicz A, Verma S, Bergin D.
Extrapancreatic neural plexus invasion by pancreatic carcinoma:characteristics on magnetic resonance imaging. Abdom Imaging.
2009;34:634–41.
47. Mochizuki K, Gabata T, Kozaka K, Hattori Y, Zen Y, Kitagawa
H, et al. MDCT findings of extrapancreatic nerve plexus invasion
by pancreas head carcinoma: correlation with en bloc pathological specimens and diagnostic accuracy. Eur Radiol. 2010;20:
1757–67.
48. Inagi E, Shimodan S, Amizuka H, Kigawa S, Shimizu Y, Nagashima K, et al. Pancreatic cancer initially presenting with apseudocyst at the splenic flexure. Pathol Int. 2006;56:558–62.

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