DOI:10.2214/AJR.07.3754
AJR 2008; 191:1115-1121
© American Roentgen Ray Society
Diffusion-Weighted Imaging in the Differential Diagnosis of Cystic Lesions of the Pancreas
Nagihan Inan1,
Arzu Arslan,
Gur Akansel,
Yonca Anik and
Ali Demirci
1 All authors: Department of Radiology, School of Medicine, University of
Kocaeli, 41380 Umuttepe, Kocaeli, Turkey.
Received January 30, 2008;
accepted after revision April 14, 2008.
Address correspondence to N. Inan
(inannagihan{at}ekolay.net).
Abstract
OBJECTIVE. The purpose of our study was to evaluate the value of
diffusion-weighted imaging (DWI) in the differential diagnosis of pancreatic
cysts.
SUBJECTS AND METHODS. Forty-two cysts (16 simple cysts, seven
pseudocysts, five abscesses, three hydatid cysts, two serous cystadenomas,
three mucinous cystadenomas, two mucinous cystadenocarcinomas, four cystic
degenerated adenocarcinomas) were included in this prospective study.
Single-shot spin-echo echo-planar DWI was performed with three b factors (0,
500, and 1,000 s/mm2), and apparent diffusion coefficients (ADCs)
were calculated. On DWI, the signal intensity of the cysts was visually
compared with the signal intensity of the pancreas parenchyma. For the
quantitative evaluation, cyst-to-pancreas signal intensity ratios, ADC of the
lesions, and cyst-to-pancreas ADC ratios were compared.
RESULTS. On visual evaluation, all cystic lesions were hyperintense
on DWI with b factors of 0 and 500 s/mm2. On DWI with a b factor of
1,000 s/mm2, all abscesses and hydatid and neoplastic cysts were
hyperintense, whereas most of the simple and pseudocysts were isointense.
Quantitatively, with b factors of 0 and 500 s/mm2, no statistical
significance was achieved. With a b factor of 1,000 s/mm2, the
cyst-to-pancreas signal intensity ratios of the abscesses and hydatid and
neoplastic cysts were significantly higher than those of the simple cysts and
pseudocysts. Setting the cutoff value of signal intensity ratio at 1.9, the
cyst-to-pancreas signal intensity ratio had a sensitivity of 70% and a
specificity of 90% for differentiating abscesses, hydatid cysts, and
neoplastic cysts from simple cysts and pseudocysts. The ADC and the ADC ratios
of the abscesses, hydatid cysts, and neoplastic cysts were significantly lower
than those of the simple cysts and pseudocysts.
CONCLUSION. DWI may help in the differential diagnosis of pancreatic
cysts.
Keywords: apparent diffusion coefficient • diffusion-weighted imaging • MRI • neoplastic cysts • nonneoplastic cysts • pancreas
Introduction
Cystic lesions of the pancreas encompass a wide variety of pathologic
entities, including nonneoplastic cysts (congenital simple cysts, pseudocysts,
abscesses, hydatid cysts) and various neoplastic cysts (serous cystadenomas,
mucinous cystadenomas, mucinous cystadenocarcinomas, cystic degenerated
adenocarcinomas, intraductal papillary mucinous neoplasms, and neuroendocrine
tumors) [1]. Pseudocysts
represent about 85–90% of all pancreatic cystic lesions
[2–4].
Because of the possible malignant potential of the mucinous cystic
neoplasms, cystic adeno carci nomas, and neuro endo crine tumors, careful
consideration of the differential diagnosis is mandatory to choose the optimal
treatment for each patient [5].
These cysts are often managed surgically in appropriate candidates. However,
asymptomatic simple cysts, pseudocysts, and serous cystadenomas are generally
managed non-operatively because they do not have malignant potential
[3]. Patient's age, symptoms,
and a possible history of acute or chronic pancreatitis with high-quality
imaging studies are helpful in establishing the differential diagnosis, but
there is still an overlap in the radiologic and clinical features
[1,
5]. Therefore, some pancreatic
cystic lesions can cause diagnostic confusion that may result in unnecessary
surgery or inappropriate follow-up. In this study, we evaluated the
contribution of diffusion-weighted imaging (DWI) in the differential diagnosis
of pancreatic cysts.
Subjects and Methods
Patients
Forty-two cystic lesions of the pancreas with a diameter of at least 1 cm
that were detected with any radiologic technique in 39 consecutive patients
(21 female, 18 male) between February and December 2007, were included in this
prospective study. Because of the limited resolution of the diffusion-weighted
images, lesions smaller than 1 cm in diameter were not included. Of the cysts,
16 (in 15 patients: seven female, eight male) were simple cysts, seven (six
patients: four female, two male) were pseudocysts, five (five patients: two
female, three male) were abscesses, three (two patients: one female, one male)
were hydatid cysts, two (two female patients) were serous cystadenomas, three
(three female patients) were mucinous cystadenomas, two (two patients: one
female, one male) were mucinous cystadenocarcinomas, and four (four patients:
one female, three male) were cystic degenerated adenocarcinomas. Three
patients had two cysts (two hydatid cysts in one patient, two pseudocysts in
one patient, and two simple cysts in one patient with polycystic kidney
disease). The mean patient age was 55.6 years (range, 11–79 years).
The diagnosis of nonneoplastic cysts was based on typical clinical history,
laboratory findings, MRI findings, and clinical and radiologic follow-up.
Unilocular cysts without a ductal connection or dilatation, septa, a solid
component, or calcification were considered simple cysts. In addition, all
patients with a tentative radiologic diagnosis of simple cyst showed no change
during clinical and radiologic follow-up (sonography every 3 months for
9–15 months). The diagnosis of the hydatid cysts was confirmed by
positive serology for hydatidosis (hemoagglutinin in hibition). In addition,
the diagnoses of all pancreatic abscesses were con firmed by surgery. The
diagnoses of all neoplastic cysts were confirmed histopathologically after
MRI.
This study was approved by the institutional review board and protocol
review committee. Because the tests used were part of the routine clinical
workup of these patients, informed consent was not required by the review
board. We obtained a blanket consent from all patients for the use of their
findings for research and educational purposes, with the patient privacy
secured.
MRI
All patients were examined with a 1.5-T MR scanner (Gyroscan Intera,
Philips Medical Systems) using a 4-element phased-array body coil. This system
has a maximal gradient strength of 30 mT/m and a slew rate of 150 mT/m/ms. All
patients were examined initially with the routine MRI protocol for the upper
abdomen that included unenhanced axial T1-weighted breath-hold spoiled
gradient-echo with and without fat suppression (TR/TE, 169/4.6; flip angle,
80°; number of excitations, 1), coronal and axial T2-weighted single-shot
turbo spin-echo (700/80; number of excitations, 1; turbo spin-echo factor,
72), and axial T2-weighted single-shot turbo spin-echo with fat suppression
(700/80; number of excitations, 1; turbo spin-echo factor, 72) sequences.
Subsequently, three series of axial single-shot spin-echo echo-planar DWI
(1,000/81; echo-planar imaging factor, 77; sensitizing gradients in the x,
y, and z directions) sequences were acquired using b values of
0, 500, and 1,000 s/mm2. Apparent diffusion coefficient (ADC) maps
were reconstructed from these images. Fat suppression was performed using the
spectral presaturation with inversion recovery (SPIR) technique. Subsequently,
0.1 mmol/kg of gadopentetate di me glumine (Magnevist, Bayer Schering) was
administered. Five dynamic series and an additional late phase (5th minute)
image were acquired with a T1-weighted breath-hold fast-field echo (169/4.6;
flip angle, 80°) sequence. MRI, including DWI, consisted of a multisection
acquisition with a slice thickness of 4 mm, an intersection gap of 1 mm, and
an acquisition matrix of 128 x 256. The field of view varied between 455
and 500 mm. All sequences were acquired using a partially parallel imaging
acquisition and SENSE reconstruction with a reduction factor of 2. The
scanning time of the acquisition of each DWI series during a single
breath-hold was 25 seconds.
Image Analysis
Qualitative analysis—The signal intensity of the cystic
lesions in all three DW images with b factors of 0, 500, and 1,000
s/mm2 was visually assessed compared with the signal intensity of
the pancreas using a 3-point scale as follows: 0, isointense; 1, moderately
hyperintense; and 2, significantly hyperintense. All images were independently
assessed by two radiologists who were blinded to the clinical history and
results of prior imaging studies. Results of the interpretations were
compared. In five cases for which the results differed, the final score was
reached by consensus after discussion.
Quantitative analysis—Quantitative analysis was performed
using a dedicated workstation (Dell Workstation precision 650, ViewForum
release 3.4'' system). The signal intensities of the cystic lesions and
pancreatic parenchyma were measured by one radiologist for each b factor (0,
500, and 1,000 s/mm2) using a region of interest (ROI) of the same
size. The ROI was placed centrally and its size was kept as large as possible,
covering at least two thirds of the cystic lesions, yet avoiding interference
from the surrounding tissue and major blood vessels. In addition, the ADC maps
were created automatically, and the mean ADC values of cystic lesions and
pancreas were determined on images with b factors 0 and 1,000
s/mm2. The average of three measurements was recorded as the final
signal intensity or ADC. Cyst-to-pancreas signal intensity ratio, ADC of the
cystic lesions, and cyst-to-pancreas ADC ratio were calculated.
Statistical Analysis
The lesions were categorized in two groups: Group 1 included simple cysts
and pseudocysts, and group 2 consisted of other cystic lesions, including
neoplastic cysts (serous cystadenomas, mucinous cystadenomas, mucinous cyst
adeno carcinomas, cystic degenerated adeno carcinomas), abscesses, and hydatid
cysts. For the qualitative analysis, Fisher's exact test was used to assess
the signal differences between the groups. For the quantitative evaluation,
signal intensity ratios, ADCs, and ADC ratios of cysts were compared. The
fitness of the numeric data set to normal distribution was determined using
the Kolmogorov-Smirnov test. The data were normally distributed. The Student's
t test was used to assess the differences between the two groups in
terms of signal intensity ratios, ADCs, and ADC ratios. A p value of
less than 0.05 was considered statistically significant.
To evaluate the diagnostic performance of the quantitative tests (signal
intensity ratio, ADC, and ADC ratio) and to describe the sensitivity and
specificity of the tests for differentiation of the two groups, receiver
operating characteristic (ROC) analysis was performed. The areas and standard
errors for each ROC curve were calculated using the method described by Metz
[6]. The area under the ROC
curve reflects the performance of the tests. The optimum cutoff point was
determined as the value that best discriminated between the two groups in
terms of maximum sensitivity and minimum number of false-positive results. All
statistical analyses were performed using SPSS (Statistical Package for the
Social Sciences) software.
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Fig. 1A —75-year-old woman with simple cyst of pancreas. Cyst was
unchanged during 12-month follow-up. Axial T1-weighted fast-field echo
(A) and T2-weighted turbo spin-echo (B) MR images show cyst in
body of pancreas.
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Fig. 1B —75-year-old woman with simple cyst of pancreas. Cyst was
unchanged during 12-month follow-up. Axial T1-weighted fast-field echo
(A) and T2-weighted turbo spin-echo (B) MR images show cyst in
body of pancreas.
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Fig. 1C —75-year-old woman with simple cyst of pancreas. Cyst was
unchanged during 12-month follow-up. This cyst (arrow, C)
appears hyperintense compared with pancreas on diffusion-weighted image with b
factor of 500 s/mm2 (C) and isointense relative to pancreas
on diffusion-weighted image with b factor 1,000 s/mm2
(D).
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Fig. 1D —75-year-old woman with simple cyst of pancreas. Cyst was
unchanged during 12-month follow-up. This cyst (arrow, C)
appears hyperintense compared with pancreas on diffusion-weighted image with b
factor of 500 s/mm2 (C) and isointense relative to pancreas
on diffusion-weighted image with b factor 1,000 s/mm2
(D).
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Results
Qualitative Analysis
Results of the visual evaluation of the signal intensity of the cysts in
diffusion trace images with a b factor of 1,000 s/mm2 are shown in
Table 1. On these images, the
signal intensities of group 2 were significantly higher than those of group 1
(p = 0.003). Most simple cysts and pseudocysts were isointense (Figs.
1A,
1B,
1C,
1D,
1E and
2A,
2B,
2C,
2D,
2E), whereas all of the
neoplastic cysts, hydatid cysts, and abscesses were hyperintense (Figs.
3A,
3B,
3C,
3D,
4A,
4B,
4C,
4D,
5A,
5B,
5C,
5D,
5E). Diffusion-weighted images
with a b factor of 500 s/mm2 were not helpful because all lesions
were moderately or significantly hyperintense on these images.
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Fig. 2C —17-year-old girl with pancreatic pseudocyst. Cyst appears
hyperintense compared with pancreas on diffusion-weighted image with b factor
of 500 s/mm2 (C) and isointense relative to pancreas on
image with b factor of 1,000 s/mm2 (D).
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Fig. 2D —17-year-old girl with pancreatic pseudocyst. Cyst appears
hyperintense compared with pancreas on diffusion-weighted image with b factor
of 500 s/mm2 (C) and isointense relative to pancreas on
image with b factor of 1,000 s/mm2 (D).
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Fig. 3B —53-year-old woman with serous cystadenoma of pancreas. Cyst
shows higher signal intensity than pancreas on diffusion-weighted images with
b factors of 500 s/mm2 (B) and 1,000 s/mm2
(C).
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Fig. 3C —53-year-old woman with serous cystadenoma of pancreas. Cyst
shows higher signal intensity than pancreas on diffusion-weighted images with
b factors of 500 s/mm2 (B) and 1,000 s/mm2
(C).
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Fig. 4B —54-year-old woman with mucinous cystadenoma of pancreas. Cyst
(arrow) shows higher signal intensity than pancreas on
diffusion-weighted images with b factors of 500 s/mm2 (B)
and 1,000 s/mm2 (C).
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Fig. 4C —54-year-old woman with mucinous cystadenoma of pancreas. Cyst
(arrow) shows higher signal intensity than pancreas on
diffusion-weighted images with b factors of 500 s/mm2 (B)
and 1,000 s/mm2 (C).
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Fig. 5A —73-year-old woman with mucinous cystadenocarcinoma of
pancreas. Axial T1-weighted fast-field echo (A) and T2-weighted turbo
spin-echo (B) MR images show cystic mass in body of pancreas.
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Fig. 5B —73-year-old woman with mucinous cystadenocarcinoma of
pancreas. Axial T1-weighted fast-field echo (A) and T2-weighted turbo
spin-echo (B) MR images show cystic mass in body of pancreas.
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Fig. 5C —73-year-old woman with mucinous cystadenocarcinoma of
pancreas. Cyst (arrow, C) shows higher signal intensity than
pancreas on diffusion-weighted images with b factors of 500 s/mm2
(C) and 1,000 s/mm2 (D).
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Fig. 5D —73-year-old woman with mucinous cystadenocarcinoma of
pancreas. Cyst (arrow, C) shows higher signal intensity than
pancreas on diffusion-weighted images with b factors of 500 s/mm2
(C) and 1,000 s/mm2 (D).
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Quantitative Analysis
The mean diameters of the cysts for group 1 and group 2 were 41.1 ±
36.5 mm and 40.7 ± 26.2 mm, respectively.
The results of the quantitative analysis of DWI are shown in
Table 2. With b factors of 0
and 500 s/mm2, no difference of statistical significance was
achieved (p > 0.05). With a b factor of 1,000 s/mm2,
the signal intensity ratios of group 2 were significantly higher than those of
group 1 (p = 0.025). The area under the ROC curve was 0.780 ±
0.105 for signal intensity ratio. With a cutoff value of 1.9, signal intensity
ratio had a sensitivity of 70% and a specificity of 90% for differentiation
between groups 1 and 2 (Fig.
6). With a cutoff value of 1.1, signal intensity ratio had a
sensitivity of 80% and a specificity of 65% for differentiation between groups
1 and 2. The ADCs and ADC ratios of group 2 were significantly lower than
those of group 1 (p = 0.006 and p = 0.005, respectively).
The areas under the ROC curve were 0.205 ± 0.085 and 0.190 ±
0.082 for ADC and ADC ratio, respectively. We could not obtain a sufficiently
discriminative cutoff value by the ROC analysis.
Discussion
Radiologic findings play a critical role in the characterization of
pancreatic cystic lesions as benign or malignant. The sensitivity and
specificity, as well as the detection of extrapancreatic extension, are
generally superior with MRI when compared with other imaging techniques
[7]. On conven tional MRI,
unenhanced T1-weighted fast-field echo and T2-weighted single-shot turbo
spin-echo fat-suppressed images and dyn amic gadolinium-enhanced T1-weighted
fast-field echo with fat saturation and coronal and oblique MR cholangio
pancreatography pulse sequences are useful
[8,
9].
However, the imaging features of these cystic lesions sometimes overlap.
For example, fewer than 5% of serous cyst adenomas have a few large cysts that
mimic mucinous cystic tumors
[4,
5,
10]. Despite specific clinical
history and imaging findings, pseudocysts may be radiologically
indistinguishable from mucinous cystic tumors. Hydatid cysts of the pancreas
have variable appearances depending on the stage of maturity. Sometimes the
appearance of hydatid cysts is similar to that of mucinous cystic tumors. In
these cases, the differential diagnosis of hydatid cyst is usually made by
clinical history and positive serology. In addition, other rare malignant
cystic neoplasms of the pancreas that may produce mucin (mucinous colloid
adenocarcinoma) or show a variable amount of cystic degeneration
(adenosquamous carcinoma, anaplastic carcinoma, papillary intraductal
adenocarcinoma, islet cell tumors, sarcomas, and cystic metastasis, including
renal cell carcinoma, melanoma, lung tumors, breast carcinoma, and ovarian
tumors) should also be included in the differential diagnosis of cystic
lesions [4].
DWI is becoming an important noninvasive technique in the characterization
of biologic tissues based on their water diffu sion pro perties, especially
those with high b value [11].
A few recent reports have suggested that DWI with single-shot echo-planar
imaging may be helpful in the detection of colorectal cancer
[11] and pancreatic
adenocarcinoma [12] or for
characterization of cystic lesions in the abdomen, such as simple cysts,
hydatid cysts, and the abscesses of the liver, as well as ovarian cystic
neoplasms and endometrial cysts, with high specificity and sensitivity
[13–16].
To our knowledge, the role of DWI in the differential diagnosis of pancreatic
cysts has not been reported previously.
In our study, significant differences between the signal intensity ratios
of pancreatic cysts were found only on images with a b factor of 1,000
s/mm2. The signal of the diffusion-weighted image is affected by
the diffusion coefficient and spin density as well as by T1 and T2 relaxation
times
[17–19].
At higher b values, the contribution of the T2 shine-through to the signal
intensity decreases, and tissue cellularity makes a greater contribution
[14]. Signal intensities of
all cystic lesions were high on diffusion-weighted images with lower b
factors; however, with a higher b factor (b = 1,000 s/mm2) signal
intensities of simple cysts and pseudocysts were isointense to the pancreas,
in contrast to hydatid cysts, abscesses, and neoplastic cysts, which remained
hyperintense. Therefore, the hyperintensity of abscesses, hydatid cysts, and
neoplastic cysts on 1,000 s/mm2 b factor images cannot be totally
attributed to the T2 shine-through effect. Diffusion can be quantitatively
evaluated by ADC, which is free of the T2 shine-through effect
[20]. In our series, the mean
ADCs of the abscesses, hydatid cysts, and neoplastic cysts were significantly
lower than those of pseudocysts and simple cysts (p < 0.05).
Hence, the high signal on diffusion-weighted images is due to the reduced
diffusion in abscesses, hydatid cysts, and neoplastic cysts. Differences
between the ADCs can be attributed to the differences in the cyst contents.
Because hydatid cysts [13],
abscesses [15], serous
cystadenomas [1,
21,
22], mucinous cystadenomas,
and mucinous cystadenocarcinomas
[1,
23] have a viscous content,
they have decreased ADCs. Hydatid cysts contain viscous hydatid sand that
consists of the scolices, hooklets, sodium chloride, proteins, glucose, ions,
lipids, and polysaccharides
[13]. Abscesses contain
viscous pus consisting of inflammatory cells, bacteria, necrotic tissue, and
proteinaceous exuded plasma
[15]. Serous cystadenomas are
multiseptate and multiloculate, and they contain glycogen-rich cells, protein
aceous fluid, or hemorrhage [1,
21,
22]. Mucinous cystadenomas and
mucinous cystadenocarcinomas contain viscous fluid that consists of mucin,
hemorrhage, or proteins [1,
23]. On the contrary, the
simple cysts and pseudocysts have a lower viscosity and thus a higher ADC
[23].
This study has several technical limitations. The main limitation was that
the echo-planar sequence used with a higher b value had a lower
signal-to-noise ratio, resulting in greater image distortion. In addition, the
echo-planar sequence causes anatomic distortion due to susceptibility effects
[14]. We did not use
pulse-triggered DWI. Mürtz et al.
[24] evaluated 12 patients
using a single-shot spin-echo echo-planar imaging sequence with ECG triggering
to minimize the influence of cardiac pulsation. They found that DWI without
pulse-triggering reduces the accuracy of measurements of ADCs in abdominal
organs.
The differential diagnosis of pancreatic cystic lesions is usually possible
with the combined use of specific morphologic features on imaging (size,
contours, the presence and thickness of a wall, internal structure, the
enhancement pattern, or calcification), laboratory data, and clinical
information. However, the differential diagnosis of neoplastic cysts from
simple cysts and pseudocysts may still be difficult. Our preliminary data
suggest that DWI may be helpful in this setting.
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R. Woodhams, S. Kakita, H. Hata, K. Iwabuchi, S. Umeoka, C. E. Mountford, and H. Hatabu
Diffusion-Weighted Imaging of Mucinous Carcinoma of the Breast: Evaluation of Apparent Diffusion Coefficient and Signal Intensity in Correlation With Histologic Findings
Am. J. Roentgenol.,
July 1, 2009;
193(1):
260 - 266.
[Abstract]
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Abstract
Introduction
) and 2 (
) on diffusion-weighted images with b
factor 1,000 s/mm2.