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36
Pancreatic Imaging: The Value for Surgery of Neuroendocrine Pancreatic Tumors
Bruno Niederle, Brigitte Happel, Amir Kurtaran,
Dermot O’Toole, and Wolfgang Schima
Introduction
As shown recently [1] 10% of all gastrointestinal
tumors arising from gastrointestinal neuroendocrine cells diagnosed within 1 year are localized
in the pancreas. Therefore pancreatic neuroendocrine (islet cell) tumors (PNET) are rare neoplasms and represent a heterogeneous group of
tumors with distinct functional and biological
behavior depending on clinical symptoms and
tumor size.
In contrast to former views [2] preoperative
imaging is of utmost importance and an integral part of the preoperative work up of PNETs
in order to plan the surgical procedure
adequately.
To date there is no single imaging modality
which can reliably show all PNETs. Sensitivity
and accuracy depend on the size (20 mm/
>21 mm), the biological behavior (benign/
malignant; functional/nonfunctional), and the
site (pancreas/duodenum) of the lesions. To
rule out the possibilities of imaging studies
available and to estimate their value for planning surgery, the characteristics of various
tumors have to be kept clearly in mind.
Insulinoma are the most common functional
PNET. They are in the majority small (<20 mm),
solitary, well-encapsulated, and benign. Insulinomas are almost exclusively intrapancreatic (99%)
[3, 4] and are usually homogeneously distributed
within the pancreatic gland.
Gastrinoma are by the majority small
(<20 mm), often multiple, and may be simultaneously located in the pancreas and the
duodenal wall (gastrinoma triangle; this
includes the duodenum, the pancreatic head,
and the hepatoduodenal ligament) [5]. Gastrinomas tend to occur more frequently in the
gastrinoma triangle; however, tumors are also
described in other parts of the pancreas and
an extrapancreatic localization is frequent,
ranging from 30 to 60% of cases (primaries?
lymph node metastasis?) [3, 6–9]. The majority of the tumors behave malignant and
therefore show lymph node metastases at the
time of surgery.
Glucagonoma, vipoma, and somatostatinoma
are more than 90% malignant, located in the
pancreatic body or tail, and at the time of
diagnosis are 20 mm.
The majority of nonfunctioning PNETs are
>20 mm, are located in the pancreatic head,
and are malignant.
Multiple endocrine neoplasia 1 (MEN 1) is
associated with multiple functional and nonfunctional PNETs in 40–60% and may be
documented in all parts of the pancreas. The
most common functioning tumors associated
with MEN 1 are gastrinoma (Zollinger–Ellison
syndrome, pancreatic or duodenal localization, frequently multiple) and insulinoma.
Other very rare tumors include vipoma or
glucagonoma.
J.G.H. Hubbard et al. (eds.), Endocrine Surgery, Springer Specialist Surgery Series,
DOI 10.1007/978-1-84628-881-4_36, Ó Springer-Verlag London Limited 2009
471
472
ENDOCRINE SURGERY
Size and Malignancy
‘‘Size’’ is an easily available, objective, and
important parameter used for the current
pathohistological classification [10] and for the
proposal of a new TNM staging including a
grading system [11] of PNETs and may,
together with the functional status, help to predict the biological course of the tumor. In the
majority of patients, neuroendocrine tumors
confined to the pancreas with a size 20 mm
behave ‘‘benign,’’ while tumors confined to
the pancreas but revealing a size >21 mm
assimilate an ‘‘uncertain’’ (well-differentiated
endocrine tumor) or ‘‘malignant potential’’
(well-differentiated or poorly differentiated
endocrine carcinoma). Using cross-sectional
imaging modalities these neuroendocrine
carcinomas are usually large tumors showing
invasion of adjacent organs, enlarged lymph
nodes, and metastasis to the liver [12].
A variety of preoperative (conventional
and functioning) imaging modalities for the
detection of these tumors is currently available.
Their combined application seems mandatory
to improve the preoperative evaluation of
PNETs, localizing small functioning and
nonfunctioning tumors, differentiating PNETS
from pancreatic adenocarcinoma, identifying
signs of malignancy, and evaluating metastatic
disease.
This chapter focuses on all imaging methods, discusses their diagnostic potential and
limitations, and describes a rational approach
of how to optimize the use of imaging PNETs
preoperatively to be of value for the endocrine
surgeon.
Radiological Imaging
Techniques
Transabdominal Ultrasonography
Transabdominal ultrasound (US) provides a
useful tool for the preliminary investigation
of islet tumors of the pancreas. US imaging
does not require ionizing radiation, is widely
available, noninvasive, and relatively cheap.
However, this imaging modality is an extremely
operator-dependent procedure and needs the
hand of an experienced sonographer. The
principal difficulties in detecting PNETs
with US arise because of the anatomy (see
Chapter 35) of the organ and the small size
of the tumors at the time of presentation.
Obesity, previous surgery, and overlying bowel
gas provide further obstacles to adequate
pancreatic imaging.
Initial scanning is performed with the patient
supine and in lateral decubitus position, using a
3.5- to 5-MHz probe. Ideally the patient should
fast for at least 6–8 h to reduce acoustic shadowing of the stomach, which obscures the pancreas
body and tail during US. Accordingly, wide
variations in sensitivity rates of US can be
found in the literature. The reported detection
rates vary between 23 and 79% [13–18].
The small islet tumors are usually well defined
and round or oval in shape, and although they
generally appear hypoechoic in relation to normal pancreatic tissue, they may have a hyperechoic capsule. The nonfunctioning PNETs are
easier to detect because they reach a larger size
before causing symptoms. Larger tumors may be
moderately echogenic, heterogeneous, and may
contain fluid-filled areas or cystic changes or
calcifications. In addition to its role in localizing
the primary tumor, US can be used to search
for metastases in the liver and regional lymph
nodes. Moreover, newer US techniques such as
US contrast agents may further improve the
diagnostic yield of transabdominal US. However,
transabdominal US alone is not sufficient for
localization of PNETs and staging of the disease
(Table 36.1).
Endoscopic US
Endoscopic US (EUS; also known as endosonography or echoendoscopy) plays a pivotal role
in PNET assessment especially in patients with
small and difficult-to-locate primaries or in
the ever-increasing cases of incidental findings
of nonfunctional PNETs. A multicenter study
verified the ability of EUS to localize pancreatic
PNETs in patients where transabdominal US
and CT were negative [8]. Whether these results
remain true in the era of modern multidetector
CT (MDCT) remains to be proven. However, at
least in small pancreatic cancers the superior
sensitivity and excellent negative predictive
value of EUS compared with MDCT has been
shown [19].
Table 36.1. Localization of pancreatic neuroendocrine tumors: sensitivity of transabdominal ultrasound, computed tomography, various types of angiography, and endoscopic
ultrasound
Transabdominal
ultrasound
Author [ref] Year Tumor type Sensitivity % (n) Technique Sensitivity % (n) Sensitivity % (n) Sensitivity % (n)
Galiber [15] 1988 Insulinoma 61 (28) Incremental 30 (23) 54 (26) – –
Rothmund [18] 1990 Insulinoma 39 (142) NA 33 (246) 62 (305) – –
B¨ottger [93] 1990 Insulinoma 70 (21) Incremental 73 (15) 67 (30) – –
Rosch [8] 1992 All NETs – –––– 82(37)
Aspestrand [94] 1993 All NETs – Incremental 79 (29) 72 (29) – –
Angeli [13] 1997 Insulinoma 79 (28 ) NA 45 (28) 69 (28) – –
Kuzin [16] 1998 Insulinoma 30 (78) NA 24 (38) 56 (118) 90 (17) –
Xi Chen [14] 2002 Insulinoma 30 (30) NA 63 (41) 27 (11) 90 (10) 33 (9)
Kirchhoff [65] 2003 Insulinoma 8 (13) Helical 46 (13) 69 (13) 92 (13) –
Gouya [95] 2003 Insulinoma – Multidetector
Wiesli [67] 2004 Insulinoma – Helical 59 (27) – 96 (27) –
Queiroz [17] 2006 Insulinoma 23 (64) NA 28 (64) 38 (64) 67 (64) 75 (64)
Wong [96] 2007 Insulinoma – NA 31 (13) 46 (6) 40 (14) –
Note: NA: not available; NET: neuroendocrine tumor.
Computed
tomography
Thin slice 94 (15) – – 94 (30)
Thick slice 57 (8) – –
Selective
angiography
Arterial stimulation and
venous sampling
Endoscopic
ultrasound
Sensitivity
%(n)
PANCREATIC IMAGING
473
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ENDOCRINE SURGERY
Newer methods such as EUS-contrast studies and elastography [20, 21] may enhance
EUS performance in this field. While the performance of EUS in preoperative localization
of the primary appears unquestionable (detection of loco-regional extension is also possible),itcannotremainthesoleexaminationin
tumor stage classification and should be combinedwithclassicalaxialimagingandespecially somatostatin (SST) receptor scintigraphy
(SRS) in a multidisciplinary fashion.
Tumor Characteristics at EUS
PNETs are generally hypervascular and well
limited. Typically the EUS pattern is a hypoechoic, homogeneous lesion with distinct margins
with peripheral rim enhancement (Fig. 36.1A).
(a)
Theses tumors present less frequently with a
hyperechoic or isoechoic texture, and in such
circumstances distinguishing them from adjacent parenchyma may be challenging. Cystic
PETs also exist although are in fact rare and
tend to be nonfunctional [22]. Other features
are the presence of calcifications and zones of
necrosis, the latter more usually occurring in
large nonfunctional tumors. The size and intrapancreatic distribution varies according to
tumor type.
The approach to examining the pancreas
has been described elsewhere in detail [23],
but a structured appraisal of the pancreatic
head followed by the body and tail (the latter
may require patient repositioning) should be
ensured. Upontumor detection, a detailed examination of the lesion includes exact localization
(b)
(c)
Fig. 36.1. (A) Nonfunctional PNET situated in the pancreatic body using EUS (7.5 MHz frequency). (B) Two peri-duodenal lymph
nodes (GG) measuring 12.3 and 15 mm in diameter are clearly seen at EUS in a patient with a Zollinger–Ellison syndrome. (C) Biopsy
(EUS-FNAB) under EUS guidance with a small 22 G needle (white line and box magnification) positioned in the centre of a
well-defined homogeneous hypoechoic PNET in the pancreatic body. (D) Subsequent histology with immunohistochemistry
showed a well-differentiated tumor staining positively for chromogranin A (brown staining).
(d)
475
PANCREATIC IMAGING
according to surgical anatomical landmarks; the
precise relation between the tumor and the main
pancreatic duct and other adjacent structures
should also be assessed due to the possibility
of performing limited pancreatic resection and
notable enucleation. The possibility of multiple
tumors as in patients with MEN 1 requires a
careful methodological approach. Finally, separate analysis of all lymph node stations should
be performed: peri-pancreatic, mesenteric,
hepatic hilum, pyloric, peri-gastric, and coeliac
(Fig. 36.1B). In cases of gastrinomas, the
duodenal wall – from the duodenal bulb to
the third portion of the duodenum – should
carefully be examined [9, 23] in a final step
using a high-frequency transducer (at least
12 MHz) in order to detect small tumors.
Performance of EUS in Different
Tumor Types
Noninvasive techniques yield preoperative
detection rates for small (<1 cm) insulinomas
of between 40 and 60% [24–26]. Invasive methods, while relatively sensitive [27–29] (60–80%
detection rates), have been rendered obsolete by
the performance of preoperative EUS, which in
addition is less dangerous with lower morbidity.
The characteristics at EUS of insulinomas
were recently reported by Anderson et al. in
36 tumors [30]. The majority were hypoechoic
(78%) and homogeneous (89%) and lessfrequently isoechoic (19%) or hyperechoic
(3%) [30]. The overall sensitivity of EUS in the
preoperative localization of insulinomas is
excellent (on the order of 80–90% [8, 30–36]).
The accuracy of EUS is higher than other
imaging techniques including spiral computed
tomography (CT), magnetic resonance imaging
(MRI), and SRS (Tables 36.1 and 36.3). While
SRS is highly sensitive for most other PNETs,
lack of the SST receptor, sst
of patients with insulinomas explains the low
performance in this setting [37, 38]. Another
factor influencing the results of conventional
imaging (CT, MRI, and SRS) stems from the
small size of these tumors [3]. EUS is therefore
the preoperative reference examination in cases
of suspicion of insulinoma and should be
combined with perioperative detection methods
(US and palpation). EUS also allows the precise
localization of the tumor within the pancreatic
subtype in 50%
2
parenchyma and will help decide whether the
tumor is amenable to a limited resection
technique.
As for insulinomas, invasive techniques have
become almost obsolete in gastrinomas and do
not allow for accurate distinction between a
duodenal and pancreatic origin [23, 39]. Few
prospective studies are available examining the
performance of EUS compared with other imaging methods. In addition, interpretation of
results is often difficult due to the lack of information concerning a duodenal localization and
the absence of a confirmed anatomical site in
certain reports [8, 31, 33, 40]. Gastrinomas are
almost exclusively hypoechoic and homogeneous
(97 and 97%, respectively) [30]. The overall
performance of EUS in preoperative detection of
gastrinomas is poor compared with other PNETs,
and this can be explained by the large proportion
of tumors localized within the duodenum
[30, 41]. Duodenal gastrinomas are almost always
very small and detection even by expert endosonographers rarely exceeds 50% [41]. Results in
patients with Zollinger–Ellison syndrome have
improved over the years – sensitivity passing
from 33 to 54% for duodenal localization over
a 10-year period in one recent report; corresponding figures for the detection of intrapancreatic gastrinomas are 75 and 100% over the
same period. Indeed, a normal pancreatic EUS
in this setting is a strong argument in favor
of a primary duodenal tumor. EUS should therefore always be combined with other techniques
(at least spiral CT and SRS) to improve results.
Combinations of EUS with SRS have yielded
detection rates of approximately 90% [35, 41].
The detection of small duodenal localizations
may be enhanced using standard axial video
endoscopy and intraoperative duodenal transillumination. Finally, careful appraisal for
lymph node involvement should be performed
as peritumoral lymphadenopathy is frequent
in patients with gastrinoma and their identification is possible using EUS in about half
of patients [32, 42].
Several groups have underlined the impact of
EUS in the accurate detection of sporadic GEP.
An interesting application of EUS is the screening and surveillance of MEN 1 patients as has
recently been described [43, 44]. These small
and multiple tumors render their detection
difficult using standard imaging techniques. As
shown recently [45] EUS is a more sensitive
476
ENDOCRINE SURGERY
technique for the detection and localization of
potentially malignant lesions in patients with
MEN 1 than CT or transabdominal US. In a
prospective study Kann [43] and coworkers
were able to show that PNETs are usually slowgrowing tumors with a very low risk to metastasize if smaller than 15 mm. Thus surveillance
with EUS could help planning the time for
surgical intervention. Despite the fact that EUS
is an invasive examination method and sedation
of the patient is often necessary, complications
such as bowel perforation or aspiration in diagnostic procedures are extremely rare and make
EUS a fairly safe method [46]. The incidental
detection of multiple PNETs should strongly
evoke the possibility of MEN 1 and should
prompt adequate genetic screening. Screening
for PNETs, which have a high incidence in MEN
1 (estimated recently to be approximately 53%
[40]), is currently recommended as their presence carries significant impact on survival in
these patients [47, 48]. In addition, use of accurate imaging procedures is mandatory because
of the lack of a clear genotype/phenotype
correlation. Imaging methods with adequate
resolution are required in following patients
with MEN 1 without or with PNETs 10 mm.
Furthermore, the incidence of nonfunctioning
tumors is increasingly recognized in MEN
1 populations (40–50%) [49], and screening in
such patients is even more challenging. A recent
retrospective study in asymptomatic individuals who were MEN 1 carriers revealed that
EUS detected a PET in 14 of 15 cases (93%);
12 had multiple tumors [50] and this led to
surgery in 13 patients [50]. The French endocrine tumor study group (Groupe de Tumeur
Endocrine) recently reported their prospective
experience using EUS in the screening of
asymptomatic MEN 1 individuals [49]. This
large series of 51 patients found a 55% detection
rate of PNETs; more than a third were >10 mm
at initial screening and 14% were >21 mm (the
cutoff used by this group for surgery was
20 mm). Follow-up was available for a limited
number of patients but EUS appeared to be
useful in detecting tumor modifications [49].
The performance of EUS in the detection
of other functional PNETs [51] is difficult to
appreciate owing to their rarity. However, following recent consensus guidelines [51], its use
does not appear to be of primary importance as
these tumors are frequently large and often
presenting at the metastatic stage, and diagnosis
is made using standard imaging and SRS in
specific clinical circumstances.
Biopsy Using EUS
Biopsy using EUS Fine needle aspiration biopsy(FNAB) (Fig. 36.1C) may be useful in cases of
locally advanced disease to confirm the diagnosis
[52, 53]. Although the diagnosis in the majority
of cases of functional PNET is easy (typical
symptoms coupled to standard axial imaging
and SRS), it is occasionally necessary to perform
a biopsy establishing the diagnosis in rare situations. In reality, when a pancreatic mass presents
with characteristic features of an endocrine
tumor and appears resectable, no biopsy is
indeed required. EUS–FNAB is usually required
in doubtful diagnostic cases or prior to surgery in
patients where pancreatic resection may carry
significant risk (e.g., elderly patients with a probable PNET on standard imaging and diagnostic
EUS but with negative SRS). A cytohistological
diagnosis may thus be preferable using
EUS–FNAB. EUS–FNAB carries several advantages over transabdominal US- or CT-guided
biopsy of pancreatic masses, such as proximity
to the lesion and the possibility of directing the
needle into the target lesion, even for small
lesions, under direct US control. Excellent performance in biopsy of pancreatic lesions has
been established in many series [52, 54], while
remaining a safe technique. Feasibility varies
from 90 to 98% and sampling yields adequate
tissue, on intention-to-biopsy, in 80–95% of
cases. While the diagnostic accuracy of
EUS–FNAB is around 90% for pancreatic adenocarcinoma [52, 53], figures are lower for PETs,
with figures ranging from 47 to 71% [52, 54, 55].
This appears to be due to the hemorrhagic character of endocrine tumors, which increases the
rate of false-negative biopsies [52]. Nonetheless,
in about three fourths of patients EUS–FNAB
yields a tiny tissue core biopsy where standard
histology coupled to immunohistochemistry can
be performed (Fig. 36.1D). Finally, the complication rate of EUS–FNAB is low (between 2 and
5%) and in most cases minor [56].
Intraoperative US
Intraoperative US (IOUS) is a useful technique
to make the palpating finger of the surgeon to
477
PANCREATIC IMAGING
‘‘see’’ inside the pancreas. With the lack of
gas and obesity, with high-frequency scanners,
and with often preoperatively acquired data the
sensitivity of IOUS is very high, given a good
exposition of the pancreas (down to the uncinate process and up to the very end of the tail) to
the sonographic transducer. In combination
with palpation, sensitivity has been reported
to be between 84 and 100% [15, 57]. The sensitivity for detection of individual masses in
patients with multiple tiny PNETs remains still
a challenge. These patients almost always have
MEN 1, which is apparent preoperatively.
The sonographic appearance of islet cell
tumors at IOUS is identical to that of transabdominal US. Lesions are localized as hypoechogenic
circular mass well defined from the normal
pancreatic tissue. An additional value of highfrequency IOUS is its ability to depict the precise
relationship of PNETs to the pancreatic duct and
the common bile duct, if tumor enucleation is
planned. However, with state-of-the-art preoperative imaging including multiphasic MDCT and
EUS an IOUS examination of the gland to look
for multifocal tumors is no longer routinely
necessary.
a fast, robust, and highly standardized method,
which provides good results in the vast majority
of patients. Compared with endoscopic US, it is
rather noninvasive, and not only the pancreas,
but also the liver can be evaluated.
Another advantage of MDCT is the possibility of doing the complete staging all at once, as
surrounding lymph nodes, infiltration of the
environment, as well as distant metastases
(e.g., liver metastases) can be visualized during
the multiphase CT examination [62]. PNETs are
mostly hypervascular and many of them ‘‘light
up’’ only for a very short period of time after
IV contrast material administration. Thus, a
dynamic MDCT examination is the preferred
scanning protocol comprising at least three
phases. Each scan with a modern MDCT scanner does not take more than 4–5 s, which is
important to catch the transient contrast
material blush of NET. As a ‘‘negative’’ oral
contrast agent, 1,000 ml water just before the
examination may help to distend the duodenum
(so-called hydro-CT). This advances the diagnosis of the pancreatico-duodenal tumors in or
just outside the duodenal wall and delineates the
head of the pancreas.
Intraoperative Endoscopic US
The use of minimally invasive surgery has been
expanding to the resection of PNETs; however,
intraoperative localization is the key to successful endoscopic surgery. As shown recently [58]
the prospectively use of intraoperative endoscopic US (IOEUS) identified 86% of the tumors.
In addition the US provides valuable information
regarding the tumors’ relationship to the duct
and nearby vascular structures, guiding laparoscopic surgery [58, 59–61].
Computed Tomography
New developments in CT technology have
resulted in dramatic improvements of CT
imaging of the pancreas in the last few years.
Modern multidetector (or ‘‘multislice’’) CT
(MDCT) scanners produce axial images of very
high resolution, providing the surgeon with
essential information concerning tumor localization and extent of disease. Compared with
transabdominal or endoscopic US and MRI,
MDCT appears to have several advantages. It is
Performance of CT in Different
Tumor Types
Insulinomas are usually isodense to normal
pancreatic tissue without IV contrast material
and are not seen unless there is a contour distortion. Rarely insulinomas may be hyperattenuating on precontrast images due to the
presence of calcification. Typically insulinomas
are hypervascular and demonstrate a greater
degree of enhancement thanthe normal pancreatic parenchyma during the arterial phase
(Fig. 36.2). Many of these tumors are small at
diagnosis and are therefore noncontour deforming, so it is important to perceive the vascular
blush for the diagnosis. Atypical MDCT appearances of insulinomas include hypovascular and
hypoattenuating lesions postcontrast, and cystic
or calcified masses precontrast.
Recently encouraging results of MDCT study
have been published, which reported correct
localization of more than 80% of gastrinomas
with MDCT (Fig. 36.3) [63]. However, diagnosis
of duodenal (extrapancreatic) localization has
always been one of the weaknesses of CT
478
ENDOCRINE SURGERY
(a)
(b)
(c)
Fig. 36.2. (A) Insulinoma of the pancreatic tail. Axial contrast-enhanced MDCT scan obtained in the arterial phase shows a
hyperattenuating lesion in the tail of the pancreas. (B) In the portal-venous phase the lesion is only barely visible. (C): 3D
reconstruction of the CT data set in the coronal plane (arterial phase) in the same patient depicts the small hypervascular
insulinoma to be very superficial in location.
present at the time of diagnosis. In this case,
localization of the primary tumor becomes
less important because there will be palliative
therapy instead of surgical cure. The other
functioning tumors of the pancreas (vipoma:
Fig. 36.4; glucagonoma: Fig. 36.5) are even
rarer. They tend to reach a greater size and
the majority have metastasized by the time of
presentation (Fig. 36.6A).
Most malignant PNETs demonstrate enhance-
ment characteristics similar to functional tumors.
They tend to present as well-defined masses of
large size with moderate or strong enhancement
after intravenous injection of contrast medium.
Fig. 36.3. Axial arterial-phase MDCT shows a small slightlyhyper-
dense gastrinoma in the pancreatic tail (arrow). Elevated serum
gastrin leads to marked thickening of gastric folds (arrow heads).
Other large tumors may be centrally hypoattenuating at the arterial and portal-venous phases
due to necrosis (Fig. 36.5). Imaging findings that
are useful in the differentiation of endocrine
imaging. Because a high proportion of gastrinomas are malignant, metastases may already be
tumors from ductal adenocarcinomas include
the presence of calcifications, lack of vascular
479
PANCREATIC IMAGING
(a)
(b)
(c)
Fig. 36.4. (A) MEN 1 – Axial MDCT (arterial phase) demonstrates a large hypervascular tumor of the pancreatic head with areas of
necrosis (VIPoma). (B) A second VIPoma is detected in the pancreatic tail. (C): Curved planar 3D reconstruction along the pancreatic
axis shows both tumors in one image.
(a)
Fig. 36.5. (A) Axial arterial phase of a MDCT, showing a large irregular demarcated glucagonoma of the pancreatic head with
tumor surrounding of the superior mesenteric artery. (B) Axial MDCT image of the liver shows several liver metastases with
hypervascular periphery and central necrosis in the arterial phase.
(b)