Endoscopic Ultrasound

Endoscopic Ultrasound and Neuroendocrine Tumours of the Pancreas

Annette Fritscher-Ravens

 
Department of Gastroenterology - Endoscopy Unit, St. Mary`s Hospital, Imperial College.
 
London, United Kingdom
 
Introduction
 
Neuroendocrine tumours of the pancreas
(PNET) - although rare - are the most
common endocrine neoplasms of the
abdomen. They are heterogeneous regarding
hormone production and biological behaviour,
hence causing a variety of clinical
presentations. Tumours that release ectopic
hormones cause distinct clinical syndromes
and are commonly detected by biochemical
tests. Non-functioning neuroendocrine
tumours (nPNET), however, may not present
with clinical symptoms until they produce
tumour mass effects at a late stage of tumour
growth. Because of the lack of symptoms they
are much more difficult to diagnose. Even if
an early pancreatic lesion were detected
accidentally, the differential diagnosis would
not necessarily include a non-functional
neuroendocrine tumour. Not only are these
tumours commonly detected late but they are
also more likely to be mistaken for an
exocrine pancreatic adenocarcinoma [1].
Complete surgical resection is the only
curative treatment for neuroendocrine
pancreatic tumours. The type of surgery is
dependent on the location, tumour size,
infiltration into adjacent organs and tumour
type, as different neuroendocrine tumours
have different patterns of spread (of the lesion
itself, locoregional and metastatic disease)
and behaviour. If there is only a single small
tumour with no evidence of spread it may be
suitable for pancreatic organ preserving
surgery such as enucleation or middle
segment resection rather than extensive
pancreatic resection [2, 3, 4].
A tailored surgical approach requires
adequate preoperative planning including the
best possible information on the number of
lesions, their exact size and location, relation
to adjacent vessels and organs and presence of
locoregional or distant metastases.
Preoperative localisation can, however, be
difficult, as these tumours are frequently
smaller than 2 cm in diameter.
Traditional imaging methods such as trans-
abdominal ultrasound (US), computed
tomography (CT) and magnet resonance
imaging (MRI) fail to present the necessary
information or to detect the tumour itself in
up to half of the patients.
Endoscopic ultrasound (EUS) provides high
resolution images of structures within or just
beyond the wall of the gastrointestinal tract
which allows the detection of lesions down to
0.3-0.5 cm [5]. This ability to image small
structures close to the gastrointestinal tract
cannot be matched at present by any external
imaging method despite continued technical
developments and improving resolution.
Consequently, EUS has established a role as a
powerful tool to detect and stage
gastrointestinal cancer or small lesions within
5 cm of the gut wall such as pancreatic
malignancies. It allows detailed visualisation
of the entire pancreas and is likely to be an
effective tool for localisation of
neuroendocrine pancreatic tumours. EUS
guided fine needle aspiration may provide a
cytological diagnosis in cases of doubt or for

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the diagnosis of non functioning tumours.
This review will attempt to evaluate the role
of EUS and EUS-FNA in neuroendocrine
pancreatic tumours and compare this
technique to other preoperative imaging
methods in view of the requirements
necessary for appropriate management of the
disease.
Tumour Characteristics and Pathology
Neuroendocrine tumours are rare entities with
a prevalence of 1/100,000 [6]. They are
classified into two major groups: hormone
producing functioning tumours (pPNET) and
non-functioning tumours (nPNET). The
frequency of insulinomas, nPNET and
gastrinomas is about the same and these are
two to eight times as common as VIPomas
and 17-30 times as common as glucagonomas
[1, 6].
More than 50% of pPNET produce more than
one hormone, when analysed by
immunocytochemistry [7, 8, 9]. Although
multiple peptides may be produced, only one
is usually biologically active and released in
sufficient quantity to cause symptoms [1].
Because multiple hormones may be present in
PNET it can be difficult - if not impossible -
to determine by immunocytochemistry which
of the hormones is clinically relevant. The
diagnosis should be made from the clinical
symptoms and measurement of secretory
products (Table 1). Even nPNET, which make
up 15-30% of cases, may elaborate hormones
[10]. The lack of clinical symptoms is due to
insufficient peptide production, insufficient
release, or concurrent secretion of inhibitory
peptides by the tumour.
It is difficult to classify PNET into benign or
malignant disease in all cases except
insulinomas which usually remain benign.
The histological classification has failed to
predict the growth pattern or malignancy [9].
Malignancy can only reliably be defined by
the presence of metastatic disease while
benign disease can only be defined by long
term clinical follow-up [8, 9].
There is a correlation between size and
malignancy, whereas size is not relevant for
the severity of hormonal symptoms [9, 11].
Insulinomas and gastrinomas tend to present
as small tumours but may be multifocal
(Figures 1 and 2) [12, 13]. Other than
pancreatic adenocarcinomas (Figure 3) or
focal chronic pancreatitis all of these tumours
are hypervascular which may be used for
differential diagnosis (Figure 4).
Table 1. Neuroendocrine tumours of the pancreas, their clinical symptoms and biochemistry used for diagnosis.
Tumor name
Clinical symptoms
Biochemical analysis
Insulinoma
Hypoglycaemia
Blood glucose levels, elevated plasma insulin
Gatrinoma
(Zollinger Ellison)
Abdominal pain, diarrhoea
Gastrin
VIPoma
(Verner-Morrison)
Watery diarrhoea, hypokalaemia
Vasoactive intestinal polipeptide (VIP)
Glucagonoma
Anaemia, glucose intolerance,
diabetes, weight loss
Glucagon
Somatostatinoma
Diabetes, diarrhoea, steatorrhoea,
cholelithiasis
Somatostatin
GHRFoma
Acromegaly
Growth hormone releasing factor (GHRF)
ACTHoma
Cushing syndrome
ACTH
PNET causing carcinoid
syndromes and hypocalcaemia
Diarrhoea, flushing symptoms of
hypercalcaemia
Serotonin, prostaglandine, parathyreoid
hormone releasing peptide (PTHP)
nPNET
Asymptomatic, weight loss,
abdominal mass
No hormone elevation

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Tumour Location
As the tumours may be very small, it can be
difficult to detect their exact location.
Appropriate treatment, however, is only
possible when sufficient information about
the primary tumour location and tumour
extent is available. As surgery is the only
curative treatment possible locoregional or
liver metastases need to be defined
preoperatively. Various conventional imaging
modalities are used to achieve this goal.
Abdominal US, CT and MRI
Most of the insulinomas and gastrinomas are
0.5-2 cm in diameter and are frequently
missed by US, CT or MRI (Figures 1 and 2).
In recent studies results of all three imaging
techniques vary from 9 to 48% in the
Figure 3. Two-cm echopoor lesion in the pancreas
which proved to be an adenocarcinoma
Figure 2. EUS image of multiple insulinomas up to 15
mm in diameter (echopoor lesions) in the neck of the
pancreas.
Figure 1. EUS image of gastrinoma (TU) in the tail of
the pancreas, next to the pancreatic duct (P GANG)
and splenic vein (V.LIENALIS), measuring 1 cm in
diameter.
Figure 4. a. VIPoma in the head of the pancreas (2 cm
in diameter). b. Color Doppler image of the same
VIPoma. This demonstrates the hypervascularisation of
the neuroendocrine lesion.

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detection of these tumours [14, 15, 16].
Although most reports of US, CT and MRI
are discouraging with a sensitivity of 29-60%
for all pancreatic neuroendocrine tumours [1,
14, 15, 16], there are some reports of more
promising results in detecting PNET.
Enhanced power Doppler ultrasound (EPDU)
after injection of levovist (Schering, Berlin,
Germany) has been used in 104 patients with
suspected neuroendocrine tumours and
compared to somatostatin receptor
scintigraphy (SRS). Sensitivity for the
differentiation
of
hypervascular
neuroendocrine tumours and other pancreatic
masses was 94% for EPDU and 54% for SRS
[17].
Gouya et al. showed that it might be
important which kind of CT is used for
tumour detection [18]. Thirty-two pancreatic
insulinomas underwent preoperative CT with
dual-phase thin-section multidetector CT
(group 1), dual-phase multidetector CT
without thin sections (group 2), or sequential
CT (group 3). The diagnostic sensitivity for
group 1 was 94%, 57% for group 2, and 29%
for group 3 [18], while Fidler et al. were able
to prospectively detect only 63% of 30
patients with insulinomas using multiphase
helicalCT [19].
Although in some studies MRI does not seem
to achieve better results in localising PNET
than US and CT [14], Thoeni et al. [20] report
of 28 patients with clinically suspected islet
cell tumours. T1- and T2-weighted spin-echo
MR demonstrated these tumours in 85% of
patients [20].
However, in all these imaging modalities
neuroendocrine tumours may only be
detectable once they have grown to a certain
size.
Angiography and Scintigraphy
As all neuroendocrine tumours are
hypervascular, angiography may be more
efficient in the demonstration of those
tumours. Studies reporting sensitivities of 17-
55% do not suggest an advantage over other
less invasive imaging modalities [21, 22, 23,
24]. Selective arterial stimulation and hepatic
venous sampling (ASVS) technique using
intra-arterial calcium as the insulin
secretagogue may be more precise in the
diagnosis of insulinomas [23].
Somatostatin receptor scintigraphy (SRS) has
been advocated to localise neuroendocrine
tumours in a number of studies. It has been
shown that for all neuroendocrine tumours,
except insulinomas, SRS has a high
sensitivity of up to 86% [14, 17, 25] but may
suffer from up to 12% false positive results.
In a study by Gibril et al. in 122 patients the
results of SRS changed management in 47%
of patients [25]. Comparing helical CT and
SRS Kumbasar et al. found similar sensitivity
and accuracy in detecting primary
neuroendocrine tumour for both of the
methods [26].
Endoscopic Ultrasound
As neuroendocrine tumours may occur as tiny
multiple endocrine neoplasia (MEN) [27]
standard imaging techniques such as US, CT
and MRI tend to be less reliable in their
detection. For this reason the use of
endoscopic ultrasound for the localisation of
these tumours within the pancreas has been
evaluated since the very early days of this
technique (Table 2). It has increasingly
become a routine procedure in the diagnostic
work-up of neuroendocrine tumours.
An early study by Roesch et al. [28] included
37 patients with 39 neuroendocrine tumours
measuring 0.5-2.5 cm (mean 1.5 cm). None of
the lesions was detected on US and CT. Using
EUS 82% of the tumours could be localised.
In 22 of these patients angiography was also
performed but was able to find the tumour in
only 27% [28].
Palazzo et al. [29] demonstrated the accuracy
for localising small endocrine pancreatic
tumours. Thirteen suspected insulinomas up
to 15 mm (in 79% of lesions) and 17
gastrinomas were imaged by US, CT and
EUS. Accuracy for EUS was 79%, US 7%
and CT 14% [29]. Zimmer et al. performed
EUS in 20 patients, 10 of which had
gastrinomas with a mean diameter of 2.1 cm
[14]. They were able to detect 79% of the

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gastrinomas. In the same group of patients
SRS detected 86%, and 29% were detected
with US, CT and MRI. The other 10 patients
had insulinomas with a mean diameter of 1.5
cm. EUS was able to localise 93% of these
tumours, while SRS identified only 14%, CT
21% and US and MRI were able to detect
only 7% [14]. A similarly encouraging result
especially in the localisation of insulinomas
was reported by De Angelis et al. in 1999
[22]. Eleven out of 12 insulinomas were
detected by EUS (91.6%) with an overall
sensitivity
for
various
pancreatic
neuroendocrine lesions of 87%. In the same
group of patients US was able to localise only
17% of the tumours, CT 30.4%, MRI 25%,
angiography 26.5% and SRS 15.4% [22]. The
same group evaluated unselected PNET of 14
patients and compared the results to surgery
[30]. The overall EUS ability to localise the
endocrine pancreatic tumours was 83%, while
US achieved 11%, CT 28%, MRI 27%,
angiography 29% and SRS 11% within the
same group of patients [30]. Out of 36
gastrinomas, Anderson et al. [21] have been
able to localise 100% correctly, while this
was possible in 88% of 36 insulinomas.
Angiography was performed in 14 of those
patients and detected 44% of the lesions [21].
Gress et al. [31] were able to tattoo an
otherwise undetected insulinoma with India
ink under EUS guidance using a 22 gauge
needle, which is mainly used for fine-needle
aspiration. At laparotomy, performed 5 hr
later, the surgeons were able to readily
recognise the tattooed area and tumour for
resection [31].
In addition to localising these tumours EUS
may be used to obtain a tissue diagnosis. This
may be particularly useful with non-
functioning neuroendocrine lesions, which are
otherwise difficult to diagnose preoperatively.
Especially if the lesions are small, knowledge
of the neuroendocrine nature of the tumour
might lead to enucleation rather than extended
pancreatic resection [32]. EUS with fine
needle aspiration (EUS-FNA) can provide
cytology diagnosis of most of the pancreatic
masses, even if they are as small as 5-8 mm
[32]. Neuroendocrine tumours, however,
make up only a small proportion of focal
pancreatic lesions detected on EUS. In a large
single centre study Fritscher-Ravens et al.
diagnosed only 5 neuroendocrine tumours out
of a total of 200 patients with focal pancreatic
lesions of unknown origin using EUS-FNA
[33]. Voss et al. [34] biopsied 15
neuroendocrine tumours out of a total of 99
patients. It is not clear how many of these
tumours were known to be neuroendocrine
hormone producing and how many non-
functioning prior to EUS. They found the
Table 2. Imaging technique used for the localisation of pancreatic neuroendocrine tumours.
Publication
No. of cases
EUS
US
CT
MRI
SRS
Angio
Roesch, 1992 [28]
38
82%
Not seen Not seen
-
-
27%
Palazzo, 1993 [29]
30
Gastrinoma: 7/9
Insulinoma: 79
0
7%
0
14%
-
-
-
Zimmer, 1996 [14]
20 (10/10)
Gastrinoma: 79%
Insulinoma: 93%
29%
7%
29%
21%
29%
7%
86%
14%
-
De Angelis, 1998 [30]
32
83%
11%
28%
27%
11%
29%
De Angelis, 1999 [22]
23
Overall: 87%
Insulinoma: 92%
17%
30%
25%
15%
27%
Bansal, 1999 [37]
36
85%
-
-
-
-
-
Anderson, 2000 [21]
72
Gastrinoma: 100%
Insulinoma: 88%
-
-
-
-
44%
Gines, 2002 [36]
10
90%
-
-
-
-
-
Gouya, 2003 [18]
30
Insulinoma: 94%
-
-
-
-
-

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results of EUS-FNA for neuroendocrine
masses less accurate (47%) than for
adenocarcinomas (81%) [34].
In a multicentre study it was shown, that the
accuracy of EUS in the detection of PNET
was significantly increased with the addition
of EUS-FNA [35]. In some cases it may be
beneficial to have additional histology proof
of the suspected nature of the tumour
although biochemical tests have shown the
presence of neuroendocrine hormones. On
ultrasound some of these tumours may
resemble a peripancreatic node (Figure 5) as
they may be attached to the pancreas just by a
small vascular stalk [21, 36]. EUS-FNA can
help to prove the nature of these lesions.
Gines et al. [36] retrospectively analysed 10
such patients who underwent EUS-FNA for
tissue proof. Sensitivity was 90% with 90%
accuracy. There were no false positive results
[36].
The cost effectiveness of EUS compared to
other imaging modalities has also been
accessed. Bansal et al. [37] compared 26
patients who underwent EUS first with 36
patients investigated before EUS became
available to this hospital. The EUS group had
significantly reduced charges for preoperative
localisation of the tumours in relation to the
non-EUS group (2,620 US$ vs. 4,846 US$).
The major cost contributor in the non-EUS
group was for angiography or venous
sampling procedures [37].
The overall advantages of endoscopic
ultrasound are that it is safe and minimally
invasive. It does not require general
anaesthesia or hospitalisation. The
complication rate including that of fine needle
aspiration is extremely low. One of the
shortcomings of EUS and EUS-FNA is that
the technique is time consuming, technically
demanding, potentially difficult and highly
operator dependent. An essential prerequisite
for performing this technique - especially in
the area of the pancreas - is familiarity with
and training in the use of radial and/or linear
array echoendoscopy. With its limited
endoscopic view and its 2-3 cm long tip on
top of the endoscope, the endoscope is not
easy to manoeuvre. As neuroendocrine
tumours of the pancreas can be very small it
may be difficult for physicians less
experienced in endoscopic ultrasound to
detect them, resulting in futile examinations.
Recent studies demonstrated that operator
experience was the essential factor in EUS-
FNA sensitivity and accuracy [38, 39]. To
enhance the chances of success in the
detection of these lesions it may be necessary
to decide for every hospital individually
which imaging modality should be used on
the basis of the available imaging techniques
and the expertise of the individuals. EUS
expertise, so far, is not readily available even
throughout the western world and training
opportunities are still limited, even if
interested physicians would be willing to
invest time and effort [39].
Despite the long learning curve for examiners
and other adversities, the effectiveness of
endoscopic ultrasound for the location and
diagnosis of neuroendocrine tumours and
locoregional lymph node metastases has been
well proven as has it’s cost effectiveness. If
liver lesions are present it may even be able to
detect those, if located in parts of the liver
visible on EUS. If there is doubt, EUS-FNA
can provide a cytological diagnosis of these
lesions and demonstrate their neuroendocrine
nature. Distant metastases, however, are not
accessible with this technique. For that
reason, some studies suggest, that EUS in
Figure 5. EUS image of a 1-cm pancreatic insulinoma.
As the lesion is located caudally and very peripheral, it
is very difficult to differentiate this primary tumour
from a locoregional lymph node.

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combination with SRS might be more
effective than either of these methods alone
[25, 40].
SRS has the advantage of being able to
examine the whole of the body and therefore
might detect multifocal disease. EUS on the
other hand might detect the tumour itself and
clarify false positive SRS results in the
duodenum, the pancreas or in the
peripancreatic region.
Conclusion
Gastrointestinal neuroendocrine tumours are
rare neoplasms that cause classic clinical
syndromes because of the excess secretion of
specific gastrointestinal hormones. The two
most important tumours clinically are
insulinomas and gastrinomas. In the
management of these patients CT and
ultrasound are the most common initial
investigations but have limited sensitivity.
Angiography, venous sampling methods and
somatostatin receptor scintigraphy are often
employed as second line investigations but
with variable success. The increased cost and
invasiveness need to be considered. SRS
appears to be a valuable imaging technique
for the detection of gastrinomas and
metastases from other neuroendocrine
tumours and has the advantage of being able
to screen the whole body.
EUS has emerged as an accurate, highly
sensitive and cost effective modality for the
preoperative localisation of pancreatic
neuroendocrine tumours. The use of the
technique for multiple endocrine tumours and
for distant metastases is, however, limited.
The combination of EUS and SRS may be
able to provide most of the information
required preoperatively and seems to be the
optimal approach available to date.
Keywords Diagnosis; Diagnostic Techniques
and Procedures; Diagnostic Techniques,
Digestive
System;
Endosonography;
Neuroendocrine Tumors; Pancreas
Abbreviations ASVS: arterial stimulation
and hepatic venous sampling; EPDU:
enhanced power Doppler ultrasound; GHRF:
growth hormone releasing factor; MEN:
multiple endocrine neoplasia; PNET:
pancreatic neuroendocrine tumours; SRS:
somatostatin receptor scintigraphy; PTHP:
parathyreoid hormone releasing peptide
Correspondence
Annette Fritscher-Ravens
Endoscopy Unit
St. Mary`s Hospital, Imperial College
London W21NY
United Kingdom
Phone: +44-776.441.2920
Fax: +44-207.886.6871
E-mail address: fri.rav@btopenworld.com
References
1. Jensen RT, Norton JA. Endocrine neoplasms of
the pancreas. In:Yamada T, ed. Textbook of
Gastroenterology. Vol. 2, 2nd ed. Philadelphia, PA,
USA: JB Lippincott, 2003:2108-46.
2. Norton JA, Fraker DL, Alexander HR, Venzon DJ,
Doppman JL, Serrano J, et al. Surgery to cure the
Zollinger-Ellison syndrome. N Engl J Med 1999;
341:635-44. [PMID 10460814]
3. Warshaw AL, Rattner DW, Fernandez-del Castillo
C, Z`graggen K. Middle segment pancreatectomy: a
novel technique for conserving pancreatic tissue. Arch
Surg 1998; 133:327-31. [PMID 9517749]
4. Wiedenmann B, Jensen RT, Mignon M, Modlin
CI, Skogseid B, Doherty G, Oberg K. Preoperative
diagnosis and surgical management of neuroendocrine
gastroenteropancreatic
tumors:
general
recommendations by a consensus workshop. World J
Surg 1998; 22:309-18. [PMID 9494425]
5. Vilmann P, Hancke S, Henriksen FW, Jacobsen
GK. Endosonographically-guided fine needle
aspiration biopsy of malignant lesions in the upper
gastrointestinal tract. Endoscopy 1993; 25:523-7.
[PMID 8287813]
6. Alexander RA, Jensen RT. Pancreatic endocrine
tumors. In: DeVita VT, Hellmann S, Rosenberg SA,
eds. Cancer. Principles and Practice of Oncology. 6th
ed. Philadelphia, PA, USA: JB Lippincott, 2001:1788.
7. Wynick D, Williams SJ, Bloom SR. Symptomatic
secondary hormone syndromes in patients with

Page 8
JOP. J Pancreas (Online) 2004; 5(4):273-281.
JOP. Journal of the Pancreas – http://www.joplink.net – Vol. 5, No. 4 – July 2004. [ISSN 1590-8577]
280
established malignant pancreatic endocrine tumors. N
Engl J Med 1988; 319:605-7. [PMID 2842676]
8. Kloppel G, Schroder S, Heitz PU. Histopathology
and immunopathology of pancreatic endocrine tumors.
In: Mignon M, Jensen RT, eds. Endoscrine Tumors of
the Pancreas: Recent Advances in Research and
Management. Series: Frontiers of Gastrointestinal
Research. Basel, Switzerland: S. Karger, 1995:99.
9. Kloppel G, Heitz PU. Pancreatic endocrine
tumors. Pathol Res Pract 1988; 183:155-68. [PMID
2898775]
10. Modlin IM, Tang LH. Approaches to the diagnosis
of gut neuroendocrine tumors: the last word (today).
Gastroenterology 1997; 112:583-90. [PMID 9024313]
11. Mignon M. Natural history of neuroendocrine
enteropancreatic tumors. Digestion 2000; 62:51-8.
[PMID 10940688]
12. Boden G. Glucagonomas and insulinomas.
Gastroenterol Clin North Am 1989; 18:831-45. [PMID
2559035]
13. Jensen RT, Gardner JD. Gastrinoma. In: Go VLW,
di Magno EP, Gardner JD, eds. The Pancreas. Biology,
Pathobiology and Disease, 2nd ed. New York, NY,
USA: Raven Press, 1993:931.
14. Zimmer T, Stolzel U, Bader M, Koppenhagen K,
Hamm B, Buhr H, et al. Endoscopic ultrasonography
and somatostatin receptor scintigraphy in the
preoperative localisation of insulinomas and
gastrinomas. Gut 1996; 39:562-8. [PMID 8944566]
15. Gibril F, Jensen RT. Comparative analysis of
diagnostic
techniques
for
localization
of
gastrointestinal neuroendocrine tumors. Yale J Biol
Med 1997; 70:509-22. [PMID 9825478]
16. Chiti A, Fanti S, Savelli G, Romeo A, Bellanova
B, Rodari M, et al. Comparison of somatostatin
receptor imaging, computed tomography and
ultrasound in the clinical management of
neuroendocrine gastro-entero-pancreatic tumours. Eur J
Nucl Med 1998; 25:1396-403. [PMID 9818279]
17. Rickes S, Unkrodt K, Ocran K, Neye H, Wermke
W. Differentiation of neuroendocrine tumors from
other pancreatic lesions by echo-enhanced power
Doppler sonography and somatostatin receptor
scintigraphy. Pancreas 2003; 26:76-81. [PMID
12499921]
18. Gouya H, Vignaux O, Augui J, Dousset B, Palazzo
L, Louvel A, et al. CT, endoscopic sonography, and a
combined protocol for preoperative evaluation of
pancreatic insulinomas. AJR Am J Roentgenol 2003;
181:987-92. [PMID 14500214]
19. Fidler JL, Fletcher JG, Reading CC, Andrews JC,
Thompson GB, Grant CS, Service FJ. Preoperative
detection of pancreatic insulinomas on multiphasic
helical CT. AJR Am J Roentgenol 2003; 181:775-80.
[PMID 12933480]
20. Thoeni RF, Mueller-Lisse UG, Chan R, Do NK,
Shyn PB. Detection of small, functional islet cell
tumors in the pancreas: selection of MR imaging
sequences for optimal sensitivity. Radiology 2000;
214:483-90. [PMID 10671597]
21. Anderson MA, Carpenter S, Thompson NW,
Nostrant TT, Elta GH, Scheiman JM. Endoscopic
ultrasound is highly accurate and directs management
in patients with neuroendocrine tumors of the pancreas.
Am J Gastroenterol 2000; 95:2271-7. [PMID
11007228]
22. De Angelis C, Carucci P, Repici A, Rizzetto M.
Endosonography in decision making and management
of gastrointestinal endocrine tumors. Eur J Ultrasound
1999; 10:139-50. [PMID 10586018]
23. Brandle M, Pfammatter T, Spinas GA, Lehmann
R, Schmid C. Assessment of selective arterial calcium
stimulation and hepatic venous sampling to localize
insulin-secreting tumours. Clin Endocrinol (Oxf) 2002;
56:149-50. [PMID 11589679]
24. Phan GQ, Yeo CJ, Hruban RH, Lillemoe KD, Pitt
HA, Cameron JL. Surgical experience with pancreatic
and peripancreatic neuroendocrine tumors: review of
125 patients. J Gastrointest Surg 1998; 2:472-82.
[PMID 9843608]
25. Gibril F, Reynolds JC, Doppman JL, Chen CC,
Venzon DJ, Termanini B, et al. Somatostatin receptor
scintigraphy: its sensitivity compared with that of other
imaging methods in detecting primary and metastatic
gastrinomas. A prospective study. Ann Intern Med
1996; 125:26-34. [PMID 8644985]
26. Kumbasar B, Kamel IR, Tekes A, Eng J, Fishman
EK, Wahl RL. Imaging of neuroendocrine tumors:
accuracy of helical CT versus SRS. Abdom Imaging
(Online) 2004; 29:3. [PMID 15162235]
27. Wamsteker EJ, Gauger PG, Thompson NW,
Scheiman JM. EUS detection of pancreatic endocrine
tumors in asymptomatic patients with type 1 multiple
endocrine neoplasia. Gastrointest Endosc 2003;
58:531-5. [PMID 14520285]
28. Rosch T, Lightdale CJ, Botet JF, Boyce GA, Sivak
MV Jr, Yasuda K, et al. Localization of pancreatic
endocrine tumors by endoscopic ultrasonography. N
Engl J Med 1992; 326:1721-6. [PMID 1317506]
29. Palazzo L, Roseau G, Chaussade S, Salmeron M,
Gaudric M, Paolaggi JA. Pancreatic endocrine tumors:
contribution of ultrasound endoscopy in the diagnosis
of localization. Ann Chir 1993; 47:419-24. [PMID
8215165]
30. De Angelis C, Repici A, Arena V, Pellicano R,
Rizzetto M. Preoperative endoscopic ultrasonography
in decision making and management for pancreatic

Page 9
JOP. J Pancreas (Online) 2004; 5(4):273-281.
JOP. Journal of the Pancreas – http://www.joplink.net – Vol. 5, No. 4 – July 2004. [ISSN 1590-8577]
281
endocrine tumors: a 6-year experience. Endoscopy
1998; 30(Suppl 1):A182-6. [PMID 9765120]
31. Gress F, Barawi M, Kim D, Grendell J.
Preoperative localization of a neuroendocrine tumor of
the pancreas with EUS-guided fine needle tattooing.
Gastrointest Endosc 2002; 55:594-7. [PMID
11923783]
32. Fritscher-Ravens A, Izbicki JR, Sriram PV, Krause
C, Knoefel WT, Topalidis T, et al. Endosonography-
guided, fine-needle aspiration cytology extending the
indication for organ-preserving pancreatic surgery. Am
J Gastroenterol 2000; 95:2255-60. [PMID 11007226]
33. Fritscher-Ravens A, Brand L, Knofel WT,
Bobrowski C, Topalidis T, Thonke F, et al.
Comparison of endoscopic ultrasound-guided fine
needle aspiration for focal pancreatic lesions in patients
with normal parenchyma and chronic pancreatitis. Am
J Gastroenterol 2002; 97:2768-75. [PMID 12425546]
34. Voss M, Hammel P, Molas G, Palazzo L, Dancour
A, O'Toole D, et al. Value of endoscopic ultrasound
guided fine needle aspiration biopsy in the diagnosis of
solid pancreatic masses. Gut 2000; 46:244-9. [PMID
10644320]
35. Ciaccia D, Harada N, Wiersema MJ, Chiappo JM,
Hoffman B, Ikenberry SO et al. Preoperative
localization and diagnosis of pancreatic and pan-
pancreatic islet cell tumors using endoscopic
ultrasound guided fine needle aspiration: a multicenter
experience. [Abstract]. Gastrointest Endosc 1997;
45:AB170.
36. Gines A, Vazquez-Sequeiros E, Soria MT, Clain
JE, Wiersema MJ. Usefulness of EUS-guided fine
needle aspiration (EUS-FNA) in the diagnosis of
functioning neuroendocrine tumors. Gastrointest
Endosc 2002; 56:291-6. [PMID 12145615]
37. Bansal R, Tierney W, Carpenter S, Thompson N,
Scheiman JM. Cost effectiveness of EUS for
preoperative localization of pancreatic endocrine
tumors. Gastrointest Endosc 1999; 49:19-25. [PMID
9869718]
38. Harewood GC, Wiersema LM, Halling AC,
Keeney GL, Salamao DR, Wiersema MJ. Influence of
EUS training and pathology interpretation on accuracy
of EUS-guided fine needle aspiration of pancreatic
masses. Gastrointest Endosc 2002; 55:669-73. [PMID
11979248]
39. Mertz H, Gautam S. The learning curve for EUS-
guided FNA of pancreatic cancer. Gastrointest Endosc
2004; 59:33-7. [PMID 14722544]
40. Cadiot G, Lebtahi R, Sarda L, Bonnaud G,
Marmuse JP, Vissuzaine C, et al. Preoperative
detection of duodenal gastrinomas and peripancreatic
lymph nodes by somatostatin receptor scintigraphy.
Groupe D'etude Du Syndrome De Zollinger-Ellison.
Gastroenterology 1996; 111:845-54. [PMID 8831579]

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