J Gastrointest Surg (2010) 14:1292–1297

DOI 10.1007/s11605-010-1221-z

SSAT POSTER PRESENTATION

An MRI-Driven Practice: a New Perspective on MRI

for the Evaluation of Adenocarcinoma of the Head
of the Pancreas
Elliot B. Tapper & Diego Martin & N. Volkan Adsay &
David Kooby & Bobby Kalb & Juan M. Sarmiento

Received: 19 December 2009 / Accepted: 28 April 2010 / Published online: 14 May 2010
# 2010 The Society for Surgery of the Alimentary Tract

Abstract
Objectives The purpose of the study was to describe the MRI-driven management of masses at the head of the pancreas.
Main outcome measures The main outcome measure was tumor resectability.
Methods A retrospective review of prospective radiographic diagnoses was undertaken.
Results Between 2004 and 2008, we have treated 124 patients for a radiographic diagnosis of adenocarcinoma of the head
of the pancreas. This diagnosis was correct in 96.0% of the time. MRI was 100% sensitive in determining resectability,
73.2–78.9% specific, and had an overall accuracy of 86.3–87.5%. MRI could detect venous and arterial involvement with
95% and 95.9% accuracy, respectively, and missed only six metastases.
Conclusion MRI is a useful tool in the preoperative imaging of pancreatic head lesions that is highly sensitive and very
specific for resectable disease. Prospective trials of MRI in this setting are indicated.

Keywords Pancreas . Adenocarcinoma . Pancreatic cancer . Introduction

Cancer imaging . MRI . Pancreaticoduodenectomy . Head of
the pancreas Pancreatic cancer famously presents late in its natural
history with a 15% chance of being amenable to resection.1
Some patients, however, arrive in time for a pancreatico-
This paper is the manuscript of a poster presentation at SSAT 2009 duodenectomy—the Whipple—which offers the only po-
(DDW, Chicago, IL, USA). tential cure for malignant lesions in or around the head of
E. B. Tapper the pancreas. For these patients, we strive for an imaging
Department of Medicine, Beth Israel Deaconess Medical Center, modality that can discern the resectable from unresectable
Boston, MA, USA
and the benign from malignant. With the emergence of
D. Martin : B. Kalb borderline resectable disease as an accepted category,2 the
Department of Radiology, School of Medicine, Emory University, decision to operate demands raised standards for the
Atlanta, GA, USA resolution and detail of the tumor’s advancement vis-à-vis
the surrounding vasculature and potential metastasis. At the
N. V. Adsay
Department of Pathology, School of Medicine, Emory University, same time, the fact of post-operative histopathological
Atlanta, GA, USA findings of non-neoplastic disease in 5–14% of patients
begs improvement in the diagnosis of malignancy.3
D. Kooby : J. M. Sarmiento
The debate over imaging pancreatic lesions is an old
Department of Surgery, School of Medicine, Emory University,
Atlanta, GA, USA one, but it is far from over. The clinician has three major
options at his or her disposal: ultrasonography, computed
J. M. Sarmiento (*) tomography (CT), and magnetic resonance imaging (MRI).
Department of Surgery, Emory University Hospital,
In their exhaustive meta-analysis, Bipat et al found helical
1364 Clifton Road, NE, Suite H-124-C,
Atlanta, GA 30322, USA CT to be the most sensitive, with no modality more specific
e-mail: jsarmie@emory.edu than the other.4 Citing this work, some believe that the role
J Gastrointest Surg (2010) 14:1292–1297 1293

Table 1 Demographics standard is the histopathological diagnosis. Statistical

Number Age Men Women analysis was univariate, using two-tailed Student’s t tests
for continuous variables.
Unresectable 30 61.8±12.3 9 21
Borderline 41 66.0±10.3 20 21
Resectable 53 65.8±11.0 26 27 Results
Overall 124 64.6±11.1 55 69
In the 4-year period under review, 124 patients received a
radiographical diagnosis of pancreatic head adenocarcino-
for MRI in this setting is for further characterization of ma by pre-operative MRI which was classified as either
small (<1 cm) hepatic lesions found on CT.5 However, unresectable, borderline, or resectable. One hepatobiliary
Bipat’s MRI data are 8–14 years old, and their pooled surgeon (JMS) operated on 114 (92%) of these patients.
sensitivity and specificity for respectability by any modality Basic demographic characteristics are listed in Table 1.
was no greater than 83% and 82%, respectively. Crucially, While the patients with unresectable disease proceeded to a
the fear of missed metastases on CT remains widespread, biopsy in preparation for chemotherapy, the rest were
prompting some institutions to use routine staging laparos- offered the Whipple procedure. The outcomes of the
copy.6 Clearly, we have room to improve. Herein, we revisit operations performed are listed in Table 2. A basic flow
the issue of MRI for the evaluation of suspected pancreatic diagram depicts the core outcomes in Fig. 1.
cancer in a busy academic tertiary referral center.
Outcomes and Histopathology

Methods About 75% of patients were offered an operation, most of

whom, in turn, accepted. Sixty-five of 94 attempted
A retrospective review was undertaken of all MRIs Whipples proceeded to completion. Twelve patients had
administered for suspected adenocarcinoma of the head of positive margins, eight were retroperitoneal, three were
the pancreas at Emory University Hospital in the 4-year
period between December 2004 and December 2008. These
studies include all cases where MRI was utilized as the Table 2 Surgical Outcomes
primary imaging modality including the entirety of one Resectable Borderline Total
hepatobiliary surgeon’s practice. MRI was used as a policy
unless there existed a contraindication. There are no Total 53 41 94
institutional guidelines in regards to the use of diagnostic Pathology
laparoscopy. Its use is infrequent and varies between Benign 1 3 4
providers. No patients who received a pre-operative MRI Adenocarcinoma 52 38 90
received a diagnostic laparoscopy. A database was created Whipple procedure
with all patients who were evaluated and treated for this Offered 53 41 94
prospective radiographic diagnosis. Patient, tumor, and Declined 3 5 8
radiographic features were reviewed. Completed 39 26 65
The radiographic features were central to the structure of Positive margin 5 7 12
the study. In concert with the surgeons, our radiologists Positive intraoperative 2 1 3
could give one of three diagnoses: unresectable, resectable, Negative margin 34 19 53
and borderline disease. Unresectable disease is defined as Node positive 21 16 37
the presence of metastases and significant vascular invasion Aborted Whipples
or encasement that is clearly not amenable reconstructive Procedure
surgery. In this case, the diagnosis of pancreatic cancer is Hepaticojejunostomy 0 1 1
made by either by open biopsies during a palliative Double bypass 11 8 19
procedure, CT-guided biopsy, or endoscopic brushings. Exploratory laparotomy 0 1 1
Resectable denotes the absence of metastases and vascular Reasons
involvement. Borderline disease denotes those tumors Venous invasion 3 4 7
which significantly abut or compress otherwise patent Arterial invasion 3 3 6
vasculature (superior mesenteric vein, portal vein, hepatic
Metastases 5 1 6
artery, superior mesenteric artery). All radiology and
Benign pathology 0 2 2
pathology reports were those of our institution. The gold
1294
Fig. 1 Radiographic diagnoses
and operations received.
known intraoperatively, and one (neck margin) was falsely
reported as negative. Two positive margins were at the
neck; one was at the bile duct and was positive up to the
confluence. Lymph node sampling was positive for adeno-
carcinoma in 21 of 39 (53.8%) in the resectable group and
16 of 26 (61.5%) in the borderline group. Ultimately,
pathology revealed some masses to be benign: Five lesions
of the 124 evaluated (4.0%) were benign, while four of the
94 operations offered (4.3%) were for ultimately benign
pathology. Of these, four were chronic pancreatitis and one
was an arteriovenous malformation. MRI, therefore, cor-
rectly predicted adenocarcinoma in 96.0% of cases.
Resectability
Definitively, radiographic resectability communicates both
the lack of metastases and vascular involvement that is not
amenable to reconstructive surgery. We further divided
these data into the categories correspondent to the two
radiographical diagnoses offered operations: resectable and
borderline resectable. This section will discuss the operative
outcomes based on these prospective diagnoses. Beyond
two cases of benign pathology (pancreatitis), the reasons for
the aborted procedure were venous and arterial invasion as
well as metastases (please see Table 2). The statistical
analysis derived from these experiences is detailed in
Table 3.
In the radiographically resectable group, 11 (22%)
patients had truly unresectable disease and received
J Gastrointest Surg (2010) 14:1292–1297
palliative bypasses. Five patients had occult metastases
and six patients had inoperable vascular involvement. In
this group, six (10.7%) patients had significant venous
involvement—three (5.7%) requiring vascular reconstruc-
tion and three for whom the Whipple was aborted—and
three had hepatic arterial involvement—all of which
prompted double bypass procedures—that was not picked
up on MRI.
The borderline group is defined by those patients with a
degree vascular involvement deemed by the radiologist and
surgeon as amenable to operation. Here, venous involve-
ment was correctly predicted 100% (38 out of 38) of the
time, and arterial involvement was correctly predicted 93%
of the time (26 out of 28). Six patients (14.6%) in this
group required vascular reconstruction. One patient in this
group had an occult metastasis.
Thirty patients had radiographically unresectable disease
and were not offered an operation. The reasons were
usually multiple, involving some combination of frank
vascular invasion not amenable to reconstructive surgery
and hepatic metastases (present in eight patients). All
patients then underwent a biopsy in preparation for
chemotherapy. Most received a CT-guided needle aspira-
tion, while five patients were diagnosed with open biopsies
during palliative operations and one patient was diagnosed
with positive bile duct brushings. Only one patient declined
a biopsy; at follow-up a year later, the disease process was
discovered with follow-up imaging and biopsies to be
chronic pancreatitis.
J Gastrointest Surg (2010) 14:1292–1297 1295

Table 3 Statistical Analysis

Sensitivity Specificity PPV NPV Accuracy

Resectability
Borderline 100 (89.9–100) 78.9 (72–78.9) 76.5 (68.7–76.5) 100 (91.2–100) 87.5 (79.3–87.5)
Resectable 100 (92.9–100) 73.2 (66.4–73.2) 78 (72.4–78) 100 (90.7–100) 86.3 (79.3–86.3)
Overall 100 (95.4–100) 61.2 (55.2–61.2) 77.4 (73.8–77.4) 100 (90.1–100) 83.3 (78.1–83.3)
Arterial involvement
Borderline 91.3 (91.5–91.3) 100 (95.4–100) 100 (89.2–100) 96.1 (91.6–96.1) 97.2 (90.9–97.2)
Overall 80.8 (70.9–80.8) 100 (96.7–100) 100 (87.8–100) 95 (92.5–95) 95.9 (91.7–95.9)
Venous involvement
Borderline 100 (95.6–100) 100 (93.7–100) 100 (93.7–100) 100 (95.6–100) 100 (90.5–95)
Overall 87.2 (91.5–87.2) 100 (96.3–100) 100 (93.4–100) 92.4 (82.4–92.4) 95 (90.5–95)

Ninety-five percent confidence intervals in parentheses

PPV positive predictive value, NPV negative predictive value

Metastases in Table 4. There are small but insignificant differences

between the groups that had negative and positive margins,
The absence of metastases was correctly predicted 93.3% of those that were resected and aborted, those that had
the time. The six metastases found were in the liver,3 vascular invasion, but not those that had metastases.
omentum,2 and gall bladder.1 In 21 instances, it was
decided to abort the Whipple. These patients, with one
exception, received a bypass procedure to palliate their Discussion
symptoms.
We undertook this study for three core reasons. Firstly, we
Occult Metastases: Retrospective Analysis of Pre-operative sought to describe the results of an MRI-driven practice to
Imaging add a fresh perspective to the literature. Secondly, we
sought to report the value and consequences of the
Imaging was reviewed for the six patients classified as emerging radiographic diagnosis of borderline resectable
resectable by MRI that were subsequently found to have disease at our institution. Thirdly, we wanted to find in our
extra-pancreatic metastases by surgery. Of these six data whether laparoscopy has a role in our practice.
patients, two clearly demonstrated extra-pancreatic metas- Accordingly, we have three conclusions: MRI is a powerful
tases upon retrospective review of the images (one patient ally in the management of pancreatic cancer, patients with
with an omental metastasis and a second patient with a liver borderline disease ought to be treated aggressively, and
metastasis). These cases represent an error in image given the low incidence of missed metastases, the role for
interpretation as opposed to the ability of MRI to detect laparoscopy in an MRI-driven practice requires further
metastases, and a correct interpretation would have resulted study but is likely to have a marginal impact. Beyond being
in a conversion of two of these six patients from resectable the newest data on MRI in almost 8 years, our series is the
status to unresectable. The other four patients with
metastases identified at surgery (one in the gallbladder, Table 4 MRI to Operation in Days
two in the liver, and the fourth patient with an omental
Resectable Borderline
metastasis) did not have clear evidence of extra-pancreatic
disease demonstrated on MRI upon re-review. Of note, at All 7.8 (6.4) 10 (9.9)
least two of these lesions (the omental metastasis and Resected 7.7 (6.8) 8.3 (9.3)
gallbladder metastasis) were positioned in such a manner Negative margin 7.4 (7.1) 7.2 (7.0)
that they likely would also have been missed on laparo- Positive margin 9.2 (3.9) 12.9 (14.6)
scopic examination. Aborted 8.1 (5.2) 13.8 (10.0)
Metastases 7.0 (4.1) 25 (0.0)
Time to Table Venous invasion 9.7 (7.0) 12.3 (8.4)
Arterial invasion 8.3 (6.8) 13 (15.1)
We also looked that the time elapsed between the date of
imaging and operation. The results of this review are listed Standard deviations in parentheses
1296
largest in the English language and the first on MRI to
delineate outcomes for borderline resectable disease as well
as the specific sensitivities for vascular invasion.
Facing any diagnostic test is the dual burdens of
sensitivity and specificity. In practice, this means providing
the surgeon with detailed and accurate information about
the regional involvement of the tumor, the presence or
absence of metastases, and whether the tumor is malignant.
For us, a radiographic diagnosis of adenocarcinoma had a
positive predictive value of 96.0%. Only 4% of our patients
had benign pathology, a rate that is one of the lowest
reported.3 The resectability vis-à-vis the surrounding
vasculature was predicted with greater than 95% accuracy.
And the absence of metastases was predicted with 93.7%
accuracy. By comparison, in one of the largest series on
pancreatic neoplasms, CT missed between 8.4% and 14%
of metastases.6 It is a widely held belief that the principle
advantage of MRI over CT is the greater capacity for the
detection of metastases.5 We can verify that advantage, and
we have found others.
The greatest advantage of MRI is its enhanced soft tissue
contrast and therefore higher sensitivity for resectable
disease. In general, we want to give our patients the best
shot at a curative operation. At the same time, our
institution strongly supports open surgical palliation as an
option for our patients should their tumor turn out to be
ineligible for the Whipple. Accordingly, our specificity for
resectable disease was 61.2%. On the other hand, our
sensitivity for resectable disease was 100%. The impact is
clear. Of the cohort examined, all patients with potentially
resectable disease were offered an operation. Sensitivities
of up to 100% using MRI have been reported previous-
ly.4,7–10 Yet the majority of the published literature is
related to the use of CT,3–6,11,12 from which it is common
knowledge that CT is the modality of choice. The data on
MRI, however, are from small series and getting old. We
believe that there is a reason to continue investigating MRI
in this setting. Moreover, with the emergence of borderline
resectability as an accepted diagnosis2,13 and the continued
use of staging laparoscopy,6,14,15 the stakes have been
raised on our imaging modalities. The exceptional soft
tissue contrast of MRI and proven ability to find even small
metastases ought to re-focus our attention.
Our experience also confirms that the radiographic
diagnosis of borderline resectability is a meaningful one.
Compared to the resectable group, borderline resectable
patients were more likely to have positive margins (26.9%
vs. 12.8%), aborted Whipples (38.5% vs. 28.0%) and
vascular reconstructive surgery (14.6% vs. 5.7%). It has
been shown, persuasively, that there is an advantage to
treating this group aggressively, with neoadjuvant chemo-
therapy followed by a resection.2 Our study did not include
those treated with neoadjuvant therapy. As we have shown,
J Gastrointest Surg (2010) 14:1292–1297
the majority of patients with borderline resectable disease
can be treated successfully in the operating room. Still,
further studies should compare life expectancy with and
without neoadjuvant therapy.
Presently, there much debate about the role of
laparoscopy for evaluating the resectability of pancreatic
adenocarcinoma.6,14–16 The central issue here is whether
our imaging modalities are missing enough metastases to
prompt a laparoscopic evaluation before ultimately com-
mitting to a laparotomy. Our experience with an MRI-
driven practice does not, at first glance, support routine
laparoscopy. At laparotomy, only six (6.3%) of the
patients offered operations had metastases. Moreover,
two had omental metastases and one had a lesion in the
posterior wall of the gall bladder, lesions which are very
difficult to see on laparoscopy. Furthermore, our retro-
spective review of the imaging yielded two lesions missed
by human error. Accordingly, we arrive at a conservative
estimate of four (4.3%) of patients who could have been
spared a laparotomy by laparoscopy. While it is difficult to
infer conclusions about diagnostic laparoscopy from a
study that did not directly evaluate that procedure, we
have found reason to study its role in an MRI-driven
practice. A study is underway to determine the cost-
effectiveness of laparoscopy.
Incidental to our primary aims, we also found that there
are differences, albeit statistically insignificant, between the
time to surgery for our main study groups, as well as
between those with and without positive margins and
vascular invasion. This finding has two implications.
Clearly, a timely operation is crucial when dealing with
pancreatic cancer. The difference in time for those who do
and do not require reconstructive vascular surgery in our
resectable group (10 vs. 3.2 days) is illustrative. Secondly,
the reasons for the difference in time to surgery for those
with borderline resectable disease ought to be studied. This
finding could be due to chance. It could also reflect the
depth of investigation and consideration that borderline
findings prompt among the healthcare team. Or it could
also reflect an unintended psychological impact on the
patient who may hesitate in the face of the more guarded
prognosis and a daunting operation. Regardless, the time to
the operating table ought to be minimized. The impact of
this diagnosis should be studied.
Our study has limitations. While the radiographic
diagnoses are prospective, this is a fundamentally retro-
spective review. Secondly, we used different standards for
the diagnosis of adenocarcinoma. Three points in our
defense: Diagnosis in patients unsuitable for laparotomy
was made in the safest and least-invasive fashion, the
standards used are sufficient for medical oncologists to start
chemotherapy, and the interpretations of both the CT-
guided aspirates and surgical specimens were made by the
J Gastrointest Surg (2010) 14:1292–1297
same pathologists. Thirdly, the evaluation of metastases in
the unresectable group is incomplete. Save for those who
had open surgery or who had their liver metastases
biopsied, there is a non-zero risk of missing lesions in this
group that is equal to that described above for the others.
Conclusion
MRI is a powerful ally in the management of this
devastating disease, patients with borderline disease ought
to be treated aggressively, and the role for laparoscopy
ought to be studied but we have reason to doubt its utility in
an MRI-driven practice. While further studies, prospective
and otherwise, are required to further validate our findings,
there is a reason to believe in a large and expanding role for
MRI in the evaluation of pancreatic adenocarcinoma.
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