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R E S E A R C H Open Access
Apparent diffusion coefficient of pancreatic
adenocarcinoma: is there any congruity
with tumor resectability?
M. Abdel Kader
1*
, H. R. Abass
2
and M. M. Suliman
3
Abstract
Background: The accurate determination of resectability in patients with pancreatic cancer is a main goal of preoperative
imaging after diagnosis. With advances in surgical techniques, the definition of resectability is in evolution, and it is crucial
for radiologists to have an understanding of findings that are relevant to the determination of resectability. The parallel
advancements in imaging technology are aiming to improve the ability of imaging modalities to predict resectability. Fifty
patients with pancreatic ductal adenocarcinoma (PDAC) were analyzed for capability of apparent diffusion coefficient
(ADC) values to predict possible tumor resectability. The patients were classified into resectable and unresectable groups
based on magnetic resonance (MR) imaging criteria. Logistic regression analysis was used. Receiver operator characteristic
(ROC) curve was reconstructed.
Results: Out of different prognostic variables, tumor size was the only significant predictor of tumor resectability.
ROC curve analysis showed that ADC value is not a discriminator of tumor resectability (area under the curve
(AUC) = 0.5, Pvalue = 0.452).
Conclusions: In patients with pancreatic adenocarcinoma, ADC values might be unreliable for prediction of tumor
resectability in clinical practice. Low ADC value in such tumors is more attributed to fibrotic nature rather than grade of
the tumor.
Keywords: ADC, Pancreatic adenocarcinoma, Resectability
Background
Ductal adenocarcinomas account for most pancreatic ma-
lignancies. Despite recent advances in imaging and man-
agement strategies, pancreatic adenocarcinoma continues
to be one of the most common causes of cancer-related
mortality worldwide [1,2]. Due to the lack of early specific
symptoms and tendency of pancreatic adenocarcinoma to
invade adjacent structures or to metastasize at an early
stage, many patients with pancreatic cancer already have
advanced disease at the time of diagnosis resulting in a
high mortality rate [3].
Surgical resection is the only potentially curative tech-
nique for managing pancreatic cancer. However, > 80% of
patients present with disease that cannot be cured with
surgical resection [4]. High-quality multiphase imaging
can help to preoperatively distinguish between patients
eligible for curative resection and those with an unresect-
able disease [4].
MRI is a well-established reliable imaging modality for
evaluation of patients with pancreatic neoplasms that
has a great advantage of excellent soft-tissue contrast for
focal lesion detection. It allows a comprehensive analysis
of the morphological changes of pancreatic parenchyma
and pancreatic duct. However; due to adverse effects
and contraindications of contrast media, there is a great
need for another imaging modality that can give the
same valuable information [3].
Diffusion-weighted (DW) MRI is a recently introduced
abdominal MR sequence that expanded MRI capabilities,
bringing functional aspects into conventional morphologic
MRI evaluation. Modifications of water diffusion induced
by different factors acting on the extracellular and intra-
cellular spaces, such as increased cell density, edema, fi-
brosis, or altered functionality of cell membranes, can be
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
* Correspondence: Moustafa18_1970@yahoo.com
1
Department of Diagnostic Radiology, El Minia University, 103 Al Azizy Street,
Shalaby, Minya, Egypt
Full list of author information is available at the end of the article
Egyptian Journal of Radiolog
y
and Nuclear Medicin
e
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine
(2019) 50:27
https://doi.org/10.1186/s43055-019-0026-7
detected using DWI sequence. Diffusion restriction can be
also quantified through calculation of ADC values within
specific regions of interest [5].
In this study, we attempted to justify whether ADC of
pancreatic adenocarcinomas can predict the status of
tumor resectability which will be ultimately reflected
upon the plan of patient management.
Methods
This is a retrospective study that was conducted upon 50
patients with pathologically proven pancreatic adenocar-
cinoma during the period from January 2016 to December
2018. Patients who received CTH or RTH before the MRI
study time were excluded from the study.
MRI examination
The patients were examined on a 1.5 Tesla MRI scanner
(Philips Achieva, Philips Medical Systems, the Netherlands).
Phased array body coil was used. The following pulse se-
quences were obtained for all patients: T1WI: axial plane,
TR/TE 992/10 ms, slice thickness 7 mm with inter-slice gap
of 1 mm and 248 × 384 matrix; T2WI: axial or coronal
plane, TR/TE 1448/100 ms, slice thickness 7 mm with in-
ter-slice gap of 1 mm and 128 × 384 matrix; T2 SPIR (fat
sat): axial or coronal plane, TR/TE460/80, slice thickness 5
mm with inter-slice gap of 1 mm and 128 × 288 matrix;
DWI: free-breathing single-shot spin-echo-based diffusion-
weighted images in axial plane, TR/TE 2500/123 ms, slice
thickness 7 mm with inter-slice gap of 1 mm and 182 × 192
matrix: at bvalues (0, 500, 1000) followed by computer-
generated ADC mapping of the pancreas.
Image interpretation
In the beginning, qualitative assessment for conventional
and diffusion-weighted MR images was done. Images were
assessed for the presence of abnormalities of pancreatic
contour and abnormal signal intensity mass at different
parts within pancreatic tissue. The site, size, and signal in-
tensity were assessed for each identified pancreatic mass,
as well as associated biliary obstruction, regional lymph
nodes, vascular invasion, and distant metastasis. When the
lesions with no vascular encasement (< 50%), separable
from the duodenum, spleen, or left kidney, or having no
distal metastasis, it is said to be resectable lesion.
This was followed by quantitative assessment: pixel-
based ADC maps were generated on a dedicated worksta-
tion (PAXERA, Ultima), for precise placement of circular
region of interest (ROI); ROIs were placed on the exact
cut of the lesions on DWI (at bvalue 1000), thus pointing
to the exact corresponding area on ADC map. Mean ADC
values for pancreatic masses were measured.
Operative technique and details
In the resectable lesions of the pancreatic head, Whip-
ple’s operation was done (6 cases) allowing the safe re-
moval of the pancreatic head, distal stomach,
duodenum, bile duct, and gall bladder. In cases of pan-
creatic body and tail lesions, distal or sub-total pancrea-
tectomy was done (3 cases). Segmental venous resection
was done and the splenic vein is preserved. An interpos-
ition graft was used to repair the removed venous seg-
ment (3 cases). When the venous patch was needed, it
was taken from the saphenous vein of the leg (2 cases).
Also, the interposition of the venous graft was needed
and taken from the left-sided internal jugular vein of the
neck (one case). In unresectable lesions, palliative proce-
dures were done. Only the resectable lesions (15 cases)
Table 1 Descriptive and imaging characteristics of studied
patients
Group I (resectable)
(N= 15)
Group II (non-resectable)
(N= 35)
Pvalue
Age
(mean ± SD)
63 ± 8 64 ± 9 0.7
Sex
(male, %)
10/15 (67%) 22/35 (63%) 0.4
Site
(head, %)
11 (73%) 30 (85 %) 0.1
Size
(mean ± SD)
2.8 ± 2.01 3.4 ± 1.4 0.8
Table 2 Comparison between detection of the lesion at
conventional and DWI
Detection of the
lesions
Size of the
lesion
Lesions Detection
rate (%)
At conventional
image
2–7 cm 37 identified 13 not
identified
74
After adding
DWI
50 identified 100
Table 3 The associated MRI findings of unresectable lesions
Frequency Percent
Bone metastasis 4/35 11.4
Liver metastasis 6 17.1
Biliary obstruction (dilated CDB, IHBD) 27 77.1
Vascular encasement 26 74.3
Infiltration of surrounding tissue left kidney 3 8.5
LN 10 25.8
Table 4 Regression analyses for different prognostic variables
Prognostic factor Pvalue OR R
2
95% CI
Age 0.055 0.925 0.115 0.849 to 1.006
Male gender 0.367 0.812 0.078 0.634 to 1.543
Size 0.001** 1.131 0.509 0.720 to 0.974
ADC value 0.542 0.104 0.084 0.164 to 1.243
** Tumor size is the only significant predictor for tumor resectability
(P-value 0.001)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 2 of 9
were proved by surgery, while the unresectable lesions
(35 cases) were proved by biopsy (either surgical 24/35
or needle biopsy 11/35).
Statistical analysis
Descriptive data were shown as mean ± SD. Two-tail
Student’sttest was used for comparison between different
groups of the study. Logistic regression analyses were
performed for prognostic factors of resectability. Receiver
operator characteristic (ROC) curve was constructed for
diagnostic performance of ADC value to discriminate
between resectable and unresectable groups. The statistical
analyses were performed using SPSS software. Pvalue
(< 0.05) was considered statistically significant.
Results
This study included 50 patients with histopathologically
proved pancreatic adenocarcinoma. The majority of
patients were males (60 %). The mean age of patients
was 62 years (± 10). The most common clinical presenta-
tion was obstructive jaundice (33 %).
They all underwent dedicated pancreatic MRI examin-
ation for detection and characterization. The most com-
mon site for involvement was pancreatic head, representing
82 % of cases, followed by pancreatic body and tail. The
maximum diameter of lesions ranged between 2 and 7 cm
in diameter (4.3 cm ± 1.3). Most of the lesions were solid
(73%), whereas 27% of the lesions had complex mixed solid
and cystic components (Table 1).
There were 13/50 lesions that could not be detected
by conventional MRI sequences (their size is from 2 to
3 cm), but could be clearly identified upon adding DW-
MRI, raising the detection rate from 74% for conven-
tional MRI to 100% after adding the DWI (Table 2).
By DWI, 37/50 lesions (74%) showed restricted dif-
fusion, while 13/50 (26%) lesions had mixed restricted
and facilitated diffusion components. The ADC values
for studied lesions ranged between 0.9 and 1.4 ×
10
−3
mm
2
/s (1.2 ± 0.07).
The lesions were classified into two groups according
to their possible respectability, based on DW-MR im-
aging findings:
Resectable lesions. This included 15/50 (30%) patients
who had clear fat planes around SMV and SMA with no
encasement (< 180°) or infiltration to surrounding struc-
tures (spleen, left kidney, and duodenum).
Unresectable lesions. This included 35/50 (70%) pa-
tients, most of which (26/35) (74%) had an MRI evidence
of vascular (mainly SMA/celiac trunk) encasement of >
180°. Meanwhile, 8/35 (23%) patients had distant (bone/
liver) metastasis, and 3/35 (8.5%) patients had pancreatic
mass lesion infiltrating the left kidney and duodenum.
Fig. 1 ROC analysis of ADC values for predicting resectability. ADC values could not discriminate between resectable and unresectable
lesions (Pvalue 0.452)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 3 of 9
There were many associated MRI findings on studied
non-resectable lesions; the most common of them were
biliary obstruction (27/35), followed by vascular encase-
ment (26/35), representing 77.1% and 74.3% respectively
while the least common associated finding was infiltra-
tion to surrounding organs (3/35) representing 8.5%
(Table 3).
Regression analyses of different variables of resectable/
unresectable groups revealed that:
–Tumor size was the only significant predictor for
detection of unresectable lesions (Pvalue = 0.0001
and R
2
= 0.5) as shown in Table 4.
–ADC values could not discriminate between
resectable and unresectable lesions as shown by the
ROC curve analysis (Pvalue = 0.452) (Fig. 1).
Selected cases were illustrated on Figs. 2,3,4,5,
and 6
Discussion
Radiology can have a major role to play not only in baseline
assessment of pancreatic adenocarcinoma, but also it can
potentially give more details that may be prognostically im-
portant, including prediction of surgical resection [6].
Both DWI visual analysis and ADC measurement can
reliably distinguish PDAC from background pancreatic
parenchyma. Pancreatic tumors, even if small in size, al-
most invariably show diffusion restriction, presenting as
a focal high signal area on high bvalue DW images with
low signal on ADC mapping [7].
In this study, we found that the pancreatic head is the
most common site for pancreatic adenocarcinoma pre-
sented. In 41/50 cases, 11/15 are resectable lesions
(73%), and in 30/35, non-resectable lesions (85%). This
is also established in the study done by Greenlee. et al.
[8], who found that 65% of pancreatic adenocarcinomas
involved the pancreatic head and uncinate process and
15% in the body and tail. The remaining lesions were de-
tected diffusely involving the pancreas.
In our study, males are more affected than females pre-
sented in 10/15 (67%) resectable and 22/35 (63) non-re-
sectable lesions. Artinyan et al. 2008 [9]statedthatthe
anatomic location of pancreatic cancer was a prognostic
factor for survival. The age of resectable lesions was lower
than the age of the patients having unresectable lesions.
In this study, the addition of DWI to the conven-
tional MRI sequence increased significantly the tumor
detection rate. Thirteen of fifty lesions could not be
detected by conventional MRI and could clearly be
Fig. 2 A 67-year-old male patient comes complaining from left hypochondrial pain and swelling. a–cDWI and ADC maps showed truly restricted
pancreatic tail lesion extending extra-pancreatic and inseparable from the left kidney. The average ADC value from this lesion was 1.2–1.5 × 10
−3
mm
2
/s) (non-resectable lesion)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 4 of 9
detected by the addition of DWI, and their sizes
ranged between 2 and 3 cm. So, the accuracy of de-
tection raised from 74 to 100%. Park et al. [10]dem-
onstrated that the addition of DW-MR imaging to
conventional MR sequences helps increase signifi-
cantly the sensitivity of MR imaging for the detection
of small pancreatic adenocarcinoma with sensitivity
values rising from 75–76% to 96–98%.
In this research, we have many associated findings
with the non-resectable lesions such as biliary obstruc-
tion in 27/35 (77.1%), vascular encasement in 26/36
(74.3%), distant metastasis in 8/35 (22.8%), infiltration to
adjacent structures in 3/35 (8.5%), and infiltrating
spleen, duodenum, and left kidney. Jun et al. [11] stated
that the most frequent sites of metastasis form carcin-
oma of the pancreas are the lymph nodes, lung, liver, ad-
renal glands, kidney, and bone.
Elsayes et al. [12] found that associated lesions should
be described and can affect surgical decision-making.
Peritoneal nodules or the presence of ascites suggest dis-
seminated disease that would render the patient unsuit-
able for a curative resection. Also, the presence of
enlarged lymph nodes can also affect surgical resectabil-
ity and indicate a need for additional therapy.
In our study, 15/50 (30%) lesions are resectable
and 35/50 (70%) lesions are non-resectable. Whipple’s
Fig. 3 A 73-year-old female patient presented by obstructive jaundice. a–cConventional images (axial and coronal T2WI) showed isointense signal
intensity lesion involving the pancreatic head with encasement of the mesenteric vessels > 180° (yellow arrow). Dilated CBD down to its lower end (arrow
in c). d–f) DWI and ADC maps revealed truly restricted pancreatic head mass with increased brightness with increasing of the bvalue denoting its
malignant nature. The vascular encasement here appeared to be < 180° (resectable lesion). Multiple hepatic (d4)andbone(d3) deposits are detected
rendering the lesion unresectable. The ADC value of the lesion ranged from 1.0 to 1.2 × 10
−3
mm
2
/s
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 5 of 9
operation was done in 6 cases, subtotal pancreatec-
tomy in 3 cases, venous graft taken from the great
saphenous vein in 2 cases, and from the internal
jugular vein in 1 case. In non-resectable lesions,
palliative procedures were done. Chen et al. [13], on
a study done on 38 patients, found that 31 lesions
were in the head or uncinate process, 5 in the body,
and 2 in the tail. Twenty-four lesions were resectable
and underwent Whipple’s (3 cases), child operation
(13 cases), pylorus-preserving pancreaticoduodenect-
omy (7 cases), and distal pancreatectomy with splen-
ectomy (7 cases). The lesion size is less than 2 cm in
10 patients and more than 2 cm in 14 patients (2–6
cm). Unresectable lesions underwent palliative proce-
dures like choledechojejunostomy, gastrojejunostomy,
and external biliary drainage.
Fig. 4 A 55-year-old male patient comes by epigastric pain and discomfort. a–cAxial and coronal T2 fat saturation sequence showed diffusely
enlarged swollen pancreas (head, body, and tail) with heterogeneous signals and relatively preserved peri-pancreatic fat planes. The pancreatic
vessels are totally encased inside the lesion. d1–d3 DWI at multiple bvalues (0, 500, and 1000 s/mm
2
) demonstrates the increase of degree of
lesion restriction by the increased bvalue denoting the malignant nature of the lesion apart from the facilitated cystic degenerated part of the
lesion in which the signal was progressively reduced (colored arrow head). e,fADC map of the pancreas showed low signal of the lesion and
the measured ROI reflected the low ADC value (0.9–1.0 × 10
−3
mm
2
/s). Also, the mesenteric vessels are noted near totally encased within the
lesion (yellow arrow at d2 and e) (non-resectable lesion)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 6 of 9
In our study, the ADC value of both resectable and
non-resectable lesions are seen with great overlap with a
wide range and insignificant Pvalue of 0.452. The ADC
value from examined lesions ranged between 09 and 1.4
×10
−3
mm
2
/s.
Also, in this research, there is no significant difference
between the ADC values of different grades of the pan-
creatic adenocarcinomas.
The mean ADC values of pancreatic adenocarcinoma
extracted from published studies are 1.3 × 10
−3
mm
2
/s
(range 0.78 × 10
−3
mm
2
/s to 2.32 × 10
−3
mm
2
/s). In gen-
eral, most of the studies reported that the mean ADC
values of malignant pancreatic tumors were lower than
those of normal pancreatic tissues and benign lesions [14].
Barral et al. [15] and Lee et al. [16], instead, did not re-
port significant differences in ADC values between
PDACs and other solid pancreatic tumors.
In addition, a considerable overlap of ADC values in the
range of malignant lesions might be present. Moreover,
benign pancreatic lesions such as pseudocysts can show
some degree of diffusion restriction which is thought to
be due to the high viscosity of its content [17]. Thus,
quantitative ADC analysis alone may be not so accurate
for characterization of pancreatic lesions [18].
Rosenkrantz et al. [19] did not report a significant dif-
ference in the mean ADC between poorly and well/mod-
erately differentiated tumors. However, some authors
postulated that the cell density is proportional to tumor
aggressiveness as ADC values were lower in higher than
lower-grade tumors in their studies. Also, other studies
suggested a relation between tumors hyper-cellularity
and increased metastatic capacity [18].
In this study, tumor size was a significant predictor for
tumor resectability. This is logical as large tumors be-
come more in contact with blood vessels and lymphatics,
and therefore, more chance of tumor spread. Phoa et al.
reported that a tumor diameter of > 3 cm showed poor
survival after resection [20].
In fact, tumor size is a particularly important prognos-
tic factor to examine as it is included in the American
Joint Committee on Cancer (AJCC) staging of pancreatic
adenocarcinoma [21].
Fig. 5 A 70-year-old male patient presented with abdominal discomfort and pain. a,bAxial T2 fat saturation revealed just deformed contour of
pancreatic body with no detectable abnormal signal lesions. c1–c3 DWI at multiple bvalues (0, 500, and 1000 s/mm
2
). The lesion appeared with
increased restriction by elevating the bvalue (yellow arrow at c3). d,eThe pancreatic lesion showed low signal at ADC map with low ADC value
(1.1 × 10
−3
mm
2
). The lesion abuts the superior surface of the mesenteric vessels but not encase them (resectable lesion)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 7 of 9
However, it should be kept in mind that the effect of
tumor size on prognosis is largely mediated through
other biologic factors such as lymph node status and
histologic differentiation rather than merely tumor size,
especially when tumor size is < 5 cm [22].
This study had some limitations such as its retrospective
design and the relatively small number of patients within
each patient group. It is recommended to focus on clear
classification of the groups, criteria of resectability, and
ADC values and their relations to each other.
Conclusion
ADC values of PADCs might be unreliable for the pre-
diction of tumor resectability in routine clinical practice.
Low ADC value in such tumors is more attributed to fi-
brotic nature rather than grade of the tumor.
Abbreviations
ADC: Apparent diffusion coefficient; DWI: Diffusion-weighted image; DW-
MRI: Diffusion-weighted-magnetic resonance imaging; MR: Magnetic
resonance; MRI: Magnetic resonance imaging; PDAC: Pancreatic ductal
adenocarcinoma; ROC: Receiving operator characteristic; SMA: Superior
mesenteric artery; SMV: Superior mesenteric vein; SPIR: Selective partial
inversion recovery; TE: Time to echo; TR: Time of repetition
Acknowledgements
Not applicable
Authors’contributions
All authors have apprised the article and actively contributed to the work.
MAK contributed to the idea, DW-MRI, ADC map evaluation, image revision,
and final editing. HRA contributed to the data collection, revision, and edit-
ing. MMS contributed to the idea, surgical interference, and images. All au-
thors read and approved the final manuscript.
Funding
No disclosure of funding was received for this work from any organization.
Availability of data and materials
The data sets generated and/or analyzed during the current study are
available from the corresponding author on reasonable request.
Ethics approval and consent to participate
This study was approved by the Ethics Committee of El Minia University. An
informed oral consent from each patient was taken before enrollment into
the study.
Consent for publication
A written informed consent was obtained from all individuals relevant to this
research.
Competing interests
The authors declare that they have no competing interests.
Fig. 6 A 63-year-old female patient presented by obstructive jaundice. aAxial T2WI revealed bulky pancreatic head with ill-defined iso-intense
signal lesion (arrow). b1–b3 DWI at different bvalues (0, 500, and 1000 s/mm
2
) showed a well-defined restricted pancreatic head lesion with
increased restriction by increasing the bvalue (yellow arrow at b3). cADC map of the pancreas showed low ADC signal from the lesion with
intermediate ADC value (1.3 × 10
−3
mm
2
/s). The pancreatic vessels are preserved and not encased by the lesion (resectable lesion)
Abdel Kader et al. Egyptian Journal of Radiology and Nuclear Medicine (2019) 50:27 Page 8 of 9
Author details
1
Department of Diagnostic Radiology, El Minia University, 103 Al Azizy Street,
Shalaby, Minya, Egypt.
2
Department of Diagnostic Radiology, El Minia
Oncology Center, Minya, Egypt.
3
Department of Oncology Surgery, El Minia
Oncology Center, Minya, Egypt.
Received: 5 June 2019 Accepted: 30 July 2019
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