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High management impact of Ga-68 DOTATATE (GaTate) PET/CT for imaging

neuroendocrine and other somatostatin expressing tumours

Article in Journal of Medical Imaging and Radiation Oncology · February 2012

DOI: 10.1111/j.1754-9485.2011.02327.x · Source: PubMed

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Journal of Medical Imaging and Radiation Oncology 56 (2012) 40–47

RADIOLO GY—O R I G I N AL ART I C L E jmiro_2327 40..47

High management impact of Ga-68 DOTATATE (GaTate) PET/CT

for imaging neuroendocrine and other somatostatin expressing
tumours
Michael S Hofman,1,2 Grace Kong,1 Oliver C Neels,1 Peter Eu,1 Emily Hong1 and Rodney J Hicks1,2
1
Centre for Cancer Imaging, Peter MacCallum Cancer Centre, and 2Departments of Medicine & Radiology, University of Melbourne, Melbourne,
Australia

MS Hofman MBBS, FRACP; G Kong MBBS, Abstract

FRACP; OC Neels PhD; P Eu MSc; E Hong
BAppSci; RJ Hicks MBBS, MD, FRACP.
Correspondence
Dr Michael Hofman, Physician in Nuclear
Medicine & Molecular Imaging, Centre for
Cancer Imaging, Peter MacCallum Cancer
Centre, St Andrews Place, Melbourne, Vic.
3002, Australia.
Email: michael.hofman@petermac.org
Conflict of interest: None.
Submitted 27 January 2011; accepted 7 July
2011.
doi:10.1111/j.1754-9485.2011.02327.x
Introduction: Ga-68 DOTATATE (Ga-octreotate, GaTate) positron emission
tomography (PET)/CT has multiple advantages compared with conventional
and In-111 octreotide imaging for neuroendocrine tumours and other
somatostatin-receptor expressing tumours. This study assesses the manage-
ment impact of incremental diagnostic information obtained from this tech-
nique compared with conventional staging.
Methods: Fifty-nine GaTate PET/CT studies were performed over an 18-month
period (52 proven or suspected gastro-entero-pancreatic or bronchial neu-
roendocrine tumours and seven neural crest/mesenchymal tumours). A ret-
rospective blinded review was performed on the number of abnormalities (1,
2–5 or >5) within defined regions with comparison to conventional imaging to
assess incremental diagnostic information. Subsequent management impact
(high, moderate or low) was determined by clinical review and follow up to
assess pre-PET stage, treatment intent and post-PET management change.
Results: Eighty-eight percent of GaTate studies were abnormal. Compared with
conventional and In-111 octreotide imaging, additional information was pro-
vided by GaTate PET/CT in 68 and 83% of patients, respectively. Management
impact was high (inter-modality change) in 47%, moderate (intra-modality
change) in 10% and low in 41% (not assessable in 2%). High management
impact included directing patients to curative surgery by identifying a primary
site and directing patients with multiple metastases to systemic therapy.
Conclusion: GaTate PET/CT imaging provides additional diagnostic information
in a high proportion of patients with consequent high management impact.
GaTate PET/CT could replace 1In-111 octreotide scintigraphy at centres where
it is available given its superior accuracy, faster acquisition and lower radia-
tion exposure. Rapid implementation could be achieved by allowing substitu-
tional funding in the Medicare Benefit Schedule.

Key words: DOTATATE; Ga-68; octreoscan; octreotate; PET/CT;

somatostatin-receptor imaging.

can metastasise widely and can secrete hormones

Introduction
Neuroendocrine tumours (NETs) are a heterogeneous
group of neoplasms arising predominantly from endo-
crine cells in the gastrointestinal tract, pancreas or
bronchial tree with highly variable clinical behaviour.
Well-differentiated NETs typically have slow growth but
resulting in clinical symptoms which can be debilitating
and life threatening. Somatostatin receptors are found
on the cell surface of neuroendocrine organs and also in
high density in well-differentiated NET.1 Octreotide, a
long-acting somatostatin analogue, was successfully
radiolabelled in 1983, allowing somatostatin-receptor

© 2012 The Authors

40 Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists

Fig. 1. Summary of patient characteristics.
Phaeochromocytoma includes two patients
with metastatic paraganglioma. Bx: biopsy.
imaging with a nuclear medicine gamma camera.2
111
In-octreotide scintigraphy has become a key imaging
modality in staging and restaging NET.3 Other tumours,
including neural crest (phaechromocytoma, paragan-
glioma and neuroblastoma), mesenchymal and well-
differentiated brain tumours, also demonstrate high
somatostatin-receptor expression.
68
Ga-DOTA-octreotate (DOTATATE, GaTate) positron
emission tomography (PET)/CT imaging is now possible
by substituting gallium-68 instead of indium-111 and
octreotate for octreotide. 68Ga is a positron emitter and
imaged with PET, providing vastly superior imaging char-
acteristics and speed compared with conventional
gamma camera imaging with 111In. This is combined with
multi-slice computer tomography (PET/CT) facilitating
detailed anatomic correlation. 68Ga has a short half-life of
approximately 68 min minimising radiation exposure and
is convenient because it can be produced on demand
on-site using a small generator that has a shelf life of
around 12 months.4 This is contrasted by 111In, which
has a long half-life of 2.8 days and needs to be produced
in large cyclotrons, which are usually located remote
from the point of administration. The use of octreotate,
a new peptide, also provides greater affinity for
somatostatin-receptor subtype 2, which is overex-
pressed in malignancy, further enhancing the accuracy.5
This study reviews our initial clinical experience with
GaTate PET/CT with a specific focus on the management
impact associated with any incremental diagnostic infor-
mation compared with 111In-octreotide and conventional
studies.
Materials and methods
Patient characteristics
Seventy-six GaTate PET/CT studies were performed in
59 patients from June 2008 until December 2009 at the
Centre for Molecular Imaging, Peter MacCallum Cancer
Centre, Melbourne, Australia (age range 23–72, mean
50; female 64%, male 36%; 46% of patients from
© 2012 The Authors
Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists
Management impact of GaTate PET/CT
outside Melbourne metropolitan area). This included 41
patients with proven gastro-entero-pancreatic (GEP-
NET) or bronchial NET, 11 suspected GEP-NET, four
paraganglioma/phaechromocytoma, two suspected mes-
enchymal tumours in patients with oncogenic osteoma-
lacia and one esthesioneuroblastoma. Seventeen GaTate
PET/CT studies were repeated in the same patient mostly
in the setting of restaging following peptide receptor
radionuclide therapy (15); these repeat studies were not
included in analysis. Figure 1 summarises patient selec-
tion and characteristics. This study was approved by the
Peter MacCallum Ethics Committee.
Patients were recruited on the basis of clinical need
with three specific patient groups were targeted: firstly,
patients with potentially resectable primary or limited
metastatic disease on anatomical and 111In-octreotide
imaging; secondly, patients with biochemical, anatomi-
cal imaging, biopsy evidence of NET but a negative
111
In-octreotide imaging; and thirdly, patients with clear
evidence of somatostatin-receptor positive, metastatic
disease on prior imaging but in whom no primary tumour
had previously been identified, as consideration of resec-
tion of primary midgut carcinoid tumours has been rec-
ommended in treatment guidelines from both North
American and Europe.6,7 The only exception to these
clinical indications was made for interstate or country
patients in whom the greater convenience of a scanning
procedure completed in less than 90 min, compared with
the 2- to 3-day procedure associated with 111In-
octreotide imaging, enabled reduced accommodation
requirements.
GaTate production and PET/CT imaging
68
Ga was eluted using an onsite 68Ge/68Ga generator
(IDB Holland BV, Baarle-Nassau, the Netherlands), puri-
fied using a method previously described8 and trans-
ferred into a reaction vessel containing 40 mg of buffered
GaTate acetate salt (ABX, Radeberg, Germany). This
was incubated for 10 min at 120°C, purified using a
preconditioned Strata X cartridge (Phenomenex) and
41
MS Hofman et al.
sterile filtered using a Millex GV filter (Millipore). Label-
ling yields were >95% and radiochemical purity assessed
by high-performance liquid chromatography (HPLC) and
thin layer chromatography (TLC) was >99%.
A range of 165–243 MBq (mean 202 MBq) GaTate was
administered by intravenous injection followed by a 30-
to 60-min uptake period. Imaging was performed, typi-
cally from vertex to upper thighs, using a PET/CT
scanner incorporating contemporaneous PET and multi-
slice CT (Discovery STE, General Electric Medical
Systems, Milwaukee, WI, USA or Biograph 64, Siemen’s,
Knoxville, TN, USA). Low-dose CT without intravenous
contrast was utilised for anatomic correlation and
attenuation correction. Patients on long-acting soma-
tostatin analogues were requested to cease these for at
least 4 weeks prior to scanning.
Studies were reviewed with blinded scoring of the
number of abnormalities (1, 2–5 or >5) within a particu-
lar organ/region. Semi-quantitative analysis was also
performed by measuring the maximum standardised
uptake value (SUVmax), a measure of tracer uptake
normalised for injected dose and patient weight. Reports
of all available previous conventional imaging, including
contrast-enhanced CT, MRI, ultrasound, X-ray (XR) and
bone scintigraphy, were reviewed, and combined find-
ings from all these studies were scored in the same
fashion. Prior contrast-enhanced CT was performed in all
patients and MRI in 16 (27%). Similar scoring was per-
formed for prior 111In-octreotide studies. This was used
to determine incremental information provided by
GaTate PET/CT; using this scoring system if there were
more than five abnormalities within an organ, detection
of additional lesions were not considered to constitute
‘additional information’, on the basis that the treatment
of multifocal metastatic disease is unlikely to be
manifestly changed by the number of metastatic sites
detected.
42 Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists
Management impact was determined by review of
clinical history and patient follow up to determine
pre-PET/CT stage, treatment intent and subsequent
management change. This was classified as high (inter-
modality, e.g. surgery to chemotherapy), moderate
(intra-modality) or low (confirming appropriateness of
management otherwise indicated by conventional
imaging).
Results
GaTate PET/CT studies
Fifty-two of 59 (88%) of PET/CT studies demonstrated
abnormalities. There was high tumour-to-background
contrast with the average of the SUVmax within the most
intense abnormal lesion in each individual patient being
32 (range 2–104).
Additional information compared with
conventional imaging
GaTate PET/CT provided additional information com-
pared with combined findings of conventional imaging
(CT, MRI, ultrasound, XR and/or bone scintigraphy) in 40
of 59 (68%) patients. In 33 of 59 (56%), this related to
identification of disease in an additional organ or distant
nodal disease. In 17 of 59 (29%), this related to detec-
tion of additional lesions within known sites of involve-
ment. The most frequent sites of additional disease
detected on GaTate PET/CT are illustrated in Figure 2.
Prior 111In-octreotide single photon emission tomogra-
phy (SPECT) was performed in 40 of 59 (68%) patients;
55% of these utilised combined SPECT/CT. These were
performed within 3, 3–6 or >6 months preceding the
GaTate PET/CT study in 35, 25 and 40%, respectively.
GaTate PET/CT provided additional information in 33 of
Fig. 2. Additional sites of disease identified
by GaTate positron emission tomography/CT
after convetional imaging workup. Other
sites: adnexal (four), paraganglioma, spinal
canal, foot, epididymis, spleen, breast and
rectum. LN, lymph node.
© 2012 The Authors

Fig. 3. Management impact. High impact denotes an inter-modality change and moderate impact denotes an intra-modality change. Chemo, chemotherapy; IA,
intra-arterial; IV, intravenous; PET, positron emission tomography; PRRT, peptide receptor radionuclide therapy; SSA, long-acting somatostatin analogue.
40 (83%) patients. The most frequent sites of additional
information were bone (18 pt), liver (17), pancreas (15),
locoregional nodes (13), distant nodes (11), small bowel
(8), peritoneal (4) and pleural (4).
Management impact
Management impact was high (inter-modality change) in
28 (47%), moderate (intra-modality change) in 6
(10%), low in 24 (41%) and was not assessable in 1
(2%). Specific details of management impact change are
illustrated in Figure 3.
In patients who underwent 111In-octreotide imaging in
the preceding 3, 3–6 or >6 months, there was a high
management impact in 71, 40 and 50%; the greater
impact in patients imaged within a shorter time window
suggests that results have not been confounded by
disease progression between scans.
In patient who had positive (n = 29) or negative
(n = 11) 111In-octreotide imaging, high management
impact was observed in 59 and 45%, respectively. In
those with positive or negative 111In-octreotide results in
the preceding 3 months, high management impact was
observed in 78 and 60%, respectively. As the most
© 2012 The Authors
Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists
Management impact of GaTate PET/CT
frequent consequence of GaTate PET/CT scanning was to
increase the number of lesions detected, many patients
received systemic therapy rather than undergoing
surgery. In the context of documented metastatic
disease and clinical or biochemical evidence of disease,
biopsy confirmation was deemed inappropriate in most
cases. Thus, histopathological confirmation of discordant
results was not available in most patients. However, in
patients with discordant results deemed to have high
impact who proceeded to surgery (n = 5), there was only
one false positive, with other findings confirmed histo-
logically. In the one false-positive case, scanned early in
our experience, moderately increased uptake in the unci-
nate process of the pancreas was reported to be suspi-
cious for pathology. This finding was concordant with
earlier 111In-octreotide imaging and was performed to
exclude additional disease. Although we now recognise
that such uptake can be physiological, the patient under-
went surgery and histology revealed no evidence of a
NET, although the referrer remarked that the patient’s
symptoms and biochemistry improved. Uncinate process
uptake is generally not seen on 111In-octreotide imaging
but was visualised in 32% (n = 19) of patients in this
cohort and was particularly prominent in this case.
43
MS Hofman et al.
Discussion
Somatostatin-receptor scintigraphy (SRS) with 111In-
octreotide has become a key modality in imaging neu-
roendocrine and other somatostatin-receptor expressing
tumours by improving detection and guiding manage-
ment decisions.9 In addition to obtaining a two-
dimensional ‘planar’ image, it is now routine to obtain
three-dimensional cross-sectional images with SPECT.
An inherent drawback is the absence of anatomic infor-
mation precluding lesion characterisation or precise
localisation.10 This can lead to difficulty distinguishing
physiological or benign aetiology from pathological
leading to both low sensitivity and false positives.11
These limitations can be overcome with hybrid SPECT/CT
scanners, which provide exact co-registration of ana-
tomic (CT) and functional (SPECT) datasets. While evi-
dence indicates substantial benefit of hybrid-imaging
devices in NET imaging,12–18 the majority of 111In-
octreotide studies are still performed with stand-alone
SPECT equipment. Even when SPECT/CT is available,
technology varies with many devices providing only
low amplitude single slice CT. On the other hand, vir-
tually all PET scanners are combined with multi-slice CT
(PET/CT) facilitating detailed, high-resolution anatomic
correlation.
It is now possible to perform SRS with PET/CT by
substituting gallium-68 for indium-111.19 Although this
study was not designed as a head-to-head comparison of
these techniques, our results demonstrate clear superi-
orly of GaTate PET/CT compared with multi-slice 111In-
octreotide SPECT/CT, which is available at our
institution. This is primarily due to the higher sensitivity
and resolution of PET compared with SPECT technology
but is possibly also influenced by the higher
somatostatin-receptor affinity of octreotate compared
with octreotide. This facilitates detection of disease that
cannot be detected with structural imaging such as CT or
MRI due to either small size or lack of anatomic abnor-
mality (see Fig. 4). Moreover, the additional information
provided by GaTate PET/CT resulted in a high manage-
ment impact in almost half of the population studied. Our
results support findings by other investigators.20–24
GaTate PET/CT also provides an improved patient
journey by significantly decreasing the total study dura-
tion and scanning time. The study can be completed
in 60–90 min including 10- to 25-min imaging time.
This contrasts with 111In-octreotide SPECT, which takes
48–72 h to complete because of longer uptake time and
scanning time (45–90 min), and necessity for repeated
imaging at multiple time points to assist in differentiating
physiological from pathological activity. In our cohort
of tertiary referrals, nearly 50% of patients were from
outside our urban region, obviating the need for many
patients to seek nearby overnight accommodation. Fur-
thermore, GaTate is produced on-site using a generator
without the need of a cyclotron providing flexibility, in
44 Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists
contrast to 111indium, which has to be pre-ordered from
overseas. GaTate PET also results in significantly lower
radiation dose (approximately 3–4 mSv) compared with
111
In-octreotide SPECT (approximately 12 mSv).25 111In
also causes radiation damage via emission of Auger
electrons, which are not accounted for by traditional
dosimetry models.26
This study is limited by the decision to select patients
on the basis of clinical need rather than to routinely
subject consecutive patients to evaluation using 111In-
octreotide SPECT/CT as well as completing a compre-
hensive set of conventional imaging procedures. We are
cognisant that our series was influenced by a selection
bias that favoured patients likely to benefit from this new
technology by virtue of negative or equivocal 111In-
octreotide SPECT or in whom the detection of more
extensive disease than already identified could poten-
tially impact management. However, we think that this is
an appropriate patient population in whom to assess the
incremental value of what is currently a restricted and
unfunded investigation in most countries. The PET
modality is also not directly comparable to the conven-
tional SPECT study due to labelling with octreotate rather
than octreotide. It is feasible to radiolabel 111In with
octreotate or use 99mTc, which has better SPECT imaging
characteristics, although neither of these radiotracers is
in routine clinical use.
A further limitation is the lack of histological verifica-
tion of all GaTate PET/CT findings. However, this is
neither practical nor ethical, particularly in patients with
metastatic disease. Our experience in the patients who
proceeded to surgery suggests a low false-positive rate
due to the high specificity of the radiotracer for soma-
tostatin receptors combined with precise anatomic char-
acterisation. Indeed, in some patients, the gold standard
of histology may be inferior due to the potential for
sampling error (see Fig. 4). Pancreatic uncinate process
was observed in approximately one-third of patients
undergoing GaTate PET/CT and should not be misinter-
preted as pathological. Our experience indicates that this
has a curvilinear pattern often best appreciated on the
coronal view.
The strength of the study is its focus on management
impact of incremental information provided by this tech-
nique. Importantly, we demonstrated a high impact in a
patient cohort that had undergone extensive prior inves-
tigations including multiple imaging and other invasive
procedures such as endoscopic ultrasound or surgery. If
GaTate PET/CT was performed earlier in the workup of
patients with clinical or biochemical evidence of neuroen-
docrine malignancy, its impact may be even higher while
sparing the cost and morbidity of multiple investigations.
Our results demonstrated a high impact in patients with
either a negative or positive 111In-octreotide study. This
suggests that GaTate should be used instead of 111In
scintigraphy in patients likely to benefit as the impact is
high regardless of the conventional result. However, it
© 2012 The Authors
 Management impact of GaTate PET/CT

Fig. 4. Middle age woman with long-

standing history of ‘chronic pancreatitis’. At
second operation found to have sub-
centimetre hepatic metastasis with histology
demonstrating well-differentiated neuroen-
docrine tumour. Triple phase CT scan demon-
strated no abnormality apart from multiple
sclerotic bone lesions considered to be
benign bony islands (osteopoikylosis) with
prior ‘negative’ bone biopsy. 111In-octreotide
scan (top right) anterior planar and single
photon emission tomography/CT (not shown)
demonstrated a solitary left supraclavicular
nodal abnormality (blue arrow). GaTate
positron emission tomography (PET)/CT scan
(top left: anterior maximum image projec-
tion, bottom: selected axial PET/CT fusion
slices) performed 1 week later demonstrated
a pancreatic primary and sub-centimetre
liver metastasis (red arrows), and widespread
nodal and osseous metastases. The patient
subsequently underwent radionuclide
therapy with 177lutetium-octreotate.

should be noted that patients who already had wide-
spread and unresectable metastatic disease were not
referred for this scan unless for the purpose of identify-
ing a previously occult primary small bowel lesion.
Despite the availability of GaTate at our centre and
having a comparable resource cost compared with a
conventional 111In-octreotide SPECT/CT imaging in our
hands, the Medicare Benefit Schedule (MBS) currently
reimburses only the latter study. Thus, we are faced with
the dilemma of performing an inferior but funded test or
a vastly superior modality that is not reimbursable.
Given the rarity of NET, generation of sufficient data to
obtain Medicare funding for this new technology through
a submission to the Medical Services Advisory Commit-
tee is likely to require a long and expensive multicentre
trial, particularly if there were to be a requirement to
also demonstrate whether its superior diagnostic accu-
racy translates into better patient outcomes. We believe
that a feasible alternative mechanism to provide patient
access to this technology would be to simply allow sub-
stitutional funding for those situations where 111In-
octreotide SPECT is already allowed. This would allow the
medical profession to choose between the two tests on
the basis of availability and the quality of the diagnostic
information provided with no differential costs on the
provision of the scan.
Conclusions
While GaTate PET/CT represents a major advance for
patients in terms of convenience and also involves
lower radiation exposure, its major advantage comes

© 2012 The Authors

Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists 45
MS Hofman et al.
from the incremental diagnostic information that it
provides in comparison to existing technology. GaTate
PET/CT has a high management impact indicating a
major role in clinical practice of neuroendocrine and
other somatostatin-avid malignancies. It provides addi-
tional information in a high proportion of patients com-
pared with conventional imaging and could replace
111
In-octreotide imaging. GaTate PET/CT is particularly
useful to guide management in patients with an
unknown primary and should also be considered prior
to major surgical intervention to more accurately stage
patients. In such cases, the ability to avoid futile
surgery or better select systemic therapies may
provide greater efficiency and better outcomes in
health-care delivery. The major barrier for adoption is
the current lack of MBS reimbursement. A strong argu-
ment can be made for substitutional funding in insti-
tutions where this technology is available.
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© 2012 The Authors

Journal of Medical Imaging and Radiation Oncology © 2012 The Royal Australian and New Zealand College of Radiologists 47

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