incremental value of 111-in pentetreotide spect/ct fusion imaging of neuroendocrine tumors

Incremental Value of 111-InPentetreotide SPECT/CT Fusion

Imaging of Neuroendocrine Tumors
Ka Kit Wong, MBBS, John M. Cahill, MBChB, Kirk A. Frey, MD, PhD, and Anca M. Avram, MD
Ac

FrMDrAugm

ªdo

Rationale and Objectives: Hybrid single photon-emission computed tomographic (SPECT) and computed tomographic (CT) imaging for

the investigation of neuroendocrine tumors allows the fusion of functional and anatomic information in a rapid and efficient method. The aimof this study was to assess the incremental diagnostic value of 111In pentetreotide SPECT/CT imaging compared with traditional planar and

SPECT imaging with respect to lesion localization and characterization and reader confidence.

Materials and Methods: Forty-nine patients (23 male, 26 female; mean age, 56.9 years; range, 14–88 years) who underwent 111In pente-

treotide planar, SPECT, and SPECT/CT imaging were eligible for this retrospective study, including patients with suspected or confirmedcarcinoid tumors (n = 24), endocrine pancreatic tumors (n = 18), medullary thyroid cancer (n = 3), paragangliomas (n = 2), and multiple endo-

crine neoplasia type I (n = 2). Planar and SPECT images were reviewed by two blinded readers, followed by interpretation using additional

SPECT/CT images in a subsequent session. A third reader provided consensus in cases with disagreements.

Results: In 55 of 89 lesions (61.8%), 111In pentetreotide SPECT/CT imaging improved lesion localization compared to planar and SPECT

imaging; in 25 of 89 lesions (28.1%), SPECT/CT imaging changed lesion classification. In 20 of 49 patients (40.8%) for reader 1 and 14 of 49

patients (28.6%) for reader 2, 111In pentetreotide SPECT/CT imaging provided incremental diagnostic value, which was considered likely to

affect patient management in twelve of 20 and seven of 14 patients, respectively. Increased reader confidence was found in 32 of 49patients (65.3%) for both readers with uniformly high confidence after SPECT/CT interpretation.

Conclusions: Hybrid 111In pentetreotide SPECT/CT imaging provides incremental diagnostic value and greater reader confidence over

planar and SPECT imaging. This is achieved though superior lesion localization, the identification of physiologic activity, and additionalanatomic information derived from the nondiagnostic CT portion of the study.

Key Words: Neuroendocrine tumors; SPECT/CT; 111In pentetreotide scintigraphy.

ªAUR, 2010

ince its introduction almost two decades ago, somato- imaging in bone, somatostatin receptor, parathyroid, and

S statin receptor scintigraphy has become the imaging

modality of choice for the evaluation of neuroendo-

crine tumors (NETs), taking advantage of the overexpression

of somatostatin receptors at the cell membrane by this group

of neoplasms, to allow imaging with radiolabeled peptide

somatostatin analogues (1–3). Hybrid single photon-emission

computed tomographic (SPECT) and computed tomo-

graphic (CT) imaging, also referred to as transmission emis-

sion tomography or functional anatomic mapping, is a novel

technology that combines functional and structural informa-

tion in a rapid and efficient method, using integrated gamma

cameras with inline CT scanners.

A recent review found evidence for superiority of SPECT/

CT imaging over the current standard (planar and SPECT)

ad Radiol 2010; 17:291–297

om the Department of Nuclear Medicine/Radiology, University of Michiganedical Center, B1G 505 G University Hospital, 1500 E Medical Centerive, Ann Arbor, MI 48109-0028. Received August 14, 2009; acceptedgust 27, 2009. Address correspondence to: K.K.W. e-mail: [email protected]

AUR, 2010i:10.1016/j.acra.2009.08.015

adrenal scintigraphy, although it was commented that there

are limited clinical studies at present (4). The improvement

in the diagnostic performance of somatostatin receptor scinti-

graphic (SRS) SPECT/CT imaging derives from (1) superior

anatomic localization of activity (and therefore lesion charac-

terization) and (2) the application of a CTalgorithm to correct

for photon attenuation in SPECT images (4–6). The CT

component is usually nondiagnostic in quality (reduced tube

current), without contrast enhancement, although the CT

images may still provide useful structural information. The

additional radiation exposure from the low-dose CT imaging

is approximated at 2 to 4 mSv, depending on the field of view

(4). Image acquisition of both components occurs with the

patient in the same bed position. Coregistration of both

tomographic sets is immediate and more precise (because of

reduced patient movement) compared to software methods

of image coregistration or side-by-side viewing of functional

and structural information.

The purpose of this study was to report our preliminary

experience at the University of Michigan nuclear medicine

department on SRS SPECT/CT imaging for the evaluation

of NETs. In particular, we were interested in the incremental

diagnostic value over standard planar and SPECT imaging, to

291

mailto:[email protected]

mailto:[email protected]

Figure 1. No incremental diagnostic value of single photon-emission computed tomographic (SPECT)/computed tomographic (CT) imaging:additional information from SPECT/CT imaging does not change the localization or characterization of activity and does not change patient

management. Whole-body anterior-posterior planar images (a) and axial (left) and coronal (right) SPECT images (b) demonstrate extensive

multifocal 111In pentetreotide uptake in the right and left hepatic lobes consistent with neuroendocrine hepatic metastases (arrows). Axial

(left) and coronal (right) fusion SPECT/CT images (c) localize activity to multiple liver lesions with central necrosis (arrows), in a patient with carci-noid tumor.

WONG ET AL Academic Radiology, Vol 17, No 3, March 2010

determine how best to integrate this technology into our

imaging protocols.

MATERIALS AND METHODS

Forty-nine patients (23 male, 26 female; mean age, 56.9 years;

range, 14–88 years) with or with potential for NETs under-

went 111In pentetreotide planar and SPECT/CT imaging,

including patients with carcinoid tumors (n = 24), endocrine

pancreatic tumors (n = 18), medullary thyroid cancer (n = 3),

paragangliomas (n = 2), and multiple endocrine neoplasia type

I (n = 2). Histologic confirmation of NETs was obtained in 39

of 49 patients (80%) at or soon after diagnosis. The study had

internal review board approval.

Following the intravenous injection of 220 MBq 111In

pentetreotide, whole-body planar images were acquired

at 24 hours in anterior and posterior projections using

a gamma camera with parallel-hole, medium-energy colli-

mators (ECAM; Siemens Medical Solutions, Erlangen,

Germany) using two 20% energy windows centered at

172 and 245 keV, respectively. SPECT/CT images were

acquired using a hybrid gamma camera with inline CT

capability (Symbia T6; Siemens Medical Solutions) either

292

24 or 48 hours after injection. SPECT images were

acquired in a 64-step (20 s/stop), 360� noncircular orbit

and reconstructed in a 128 � 128 matrix using a three-

dimensional ordered-subsets expectation maximization

algorithm. CT correction for attenuation was applied to

SPECT images. The CT parameters used were 130 kVp

and 100 mAs, with reconstruction in a 512 � 512 matrix

at a slice thickness of 5 mm. Sixty-one regions (47 abdom-

inal, 11 thoracic, and 3 head and neck) were evaluated,

with 12 patients having SPECT/CT scans of two regions.

The SRS images were reviewed by two blinded nuclear

medicine physicians, with knowledge only of the NET

type. In the first stage of image analysis, readers independently

reviewed planar and SPECT images; identified 111In pente-

treotide avid foci and classified them according to intensity,

location, and nature (physiologic, benign, or neoplastic);

and assigned reader confidence levels using a subjective five-

point scale (1 = no confidence, 2 = equivocal, 3 = possible

disease, 4 = probable disease, 5 = certainly disease). Indium-

111 pentetreotide SPECT/CT images for each patient were

subsequently reviewed to reclassify the location and nature

of lesions and to reassess reader confidence. Incremental diag-

nostic information derived from SPECT/CT images over

Figure 2. Minor incremental diagnostic value of single photon-emission computed tomographic (SPECT)/computed tomographic (CT)

imaging: improved lesion localization and reader confidence, which is unlikely to significantly change patient management. Whole-body ante-rior-posterior planar images (a) and axial (left) and coronal (right) SPECT images (b) demonstrate a suspicious focus in the right posterior thorax,

likely in lung parenchyma (arrows). Axial low-dose CT (c) and corresponding axial fusion SPECT/CT images (d) unambiguously localize the

thoracic focus of activity to the posteromedial right lung, due to either pulmonary metastases or inflammation (arrows). Resolution of lung infil-trate on progress diagnostic CT imaging suggested post–radiation therapy inflammation in a patient undergoing restaging for medullary thyroid

cancer.

Academic Radiology, Vol 17, No 3, March 2010 111-IN PENTETREOTIDE SPECT/CT IMAGING

planar and SPECT images was broadly classified as not clini-

cally significant (no change to management; Fig 1), minor

(unlikely to affect clinical management; Fig 2), or major

(likely to affect clinical management; Fig 3). A third reader

provided consensus in cases with disagreement.

RESULTS

A total of 89 discrete 111In pentetreotide avid foci were iden-

tified, involving the head and neck (n = 8), thorax (n = 11),

liver (n = 14), extrahepatic abdomen (n = 43), and skeleton

(n = 13), and these were classified according to location and

nature (physiologic, benign, or neoplastic). A consensus

read found that SPECT/CT imaging provided superior lesion

localization in 55 of 89 lesions (61.8%), defined as a more

precise interpretation of the anatomic site of lesion activity

(Fig 4). In no circumstance did planar and SPECT images

give a more accurate location than SPECT/CT images. Of

the 55 lesions with improved localization compared to planar

and SPECT images, 24 were considered minor changes,

whereas 31 (56%) were major (defined as localization to

a different organ or an unexpected finding). SPECT/CT

imaging improved characterization in 25 of 89 lesions

(28.1%), including detecting additional sites of disease or

inflammation considered significant (n = 12) and additional

sites of disease unlikely to change management (n = 6). There

were seven lesions initially thought to represent disease, which

were clearly demonstrated by SPECT/CT imaging to be

physiologic.

Regarding scan interpretation, 32 of 49 patients had positive

findings of either somatostatin-expressing tumors or uptake by

activated macrophages due to inflammation. Seventeen

patients had negative results of 111In pentetreotide studies.

An incremental diagnostic value of SPECT/CT imaging was

found in 20 of 49 patients (40.8%) for reader 1 and 14 of 49

patients (28.6%) for reader 2, and 111In pentetreotide

SPECT/CT imaging provided incremental diagnostic value,

which was considered likely to affect patient management, in

twelve of 20 and seven of 14 patients, respectively (Table 1).

The cases with major impact included four of the 17 scans

with negative results in which initial diagnoses of disease

were correctly reassigned by SPECT/CT imaging to physio-

logic activity in the gallbladder in two patients, superficial

skin contamination in one patient, and bowel with normal

293

Figure 3. Major incremental diagnostic value of single photon-emission computed tomographic (SPECT)/computed tomographic (CT)

imaging: superior lesion localization, change in lesion characterization, and increased reader confidence, likely to significantly alter patient

management. Whole-body anterior-posterior planar images (a) and axial (left) and coronal (right) SPECT images (b) demonstrate a suspiciousfocus in the left upper quadrant (arrows) in addition to central abdominal uptake due to mesenteric lymph node disease. Axial low-dose CT (left)

and corresponding (right) axial fusion SPECT/CT images (c) demonstrate a soft tissue mass in the splenic bed (arrows), compatible with

physiologic uptake in a splenule, in a patient with a history of splenectomy.

Focal lesions(n = 89)

Focal lesions(n = 89)

No change Superior No change Change in lesion location localization lesion nature lesion nature

(n = 34) (n = 55) (n = 64) (n = 25)

Major impact Minor impact Major impact Minor impact Physiological* (n = 31) (n = 24) (n = 12) (n = 6) (n = 7)

Figure 4. Incremental diagnostic value of111In pentetreotide single photon-emissioncomputed tomographic (SPECT)/computed

tomographic (CT) imaging with respect to

lesion localization and characterization. Majorimpact: superior localization or characteriza-

tion of SPECT/CT imaging likely to change

patient management decisions. Minor impact:

change in lesion location or nature on the basisof SPECT/CT imaging unlikely to change

management options, such as an additional

site of disease in a patient with multiple metas-

tases. *SPECT/CT imaging localizedsuspicious activity to a normal structure,

confirming physiologic biodistribution.


morphology in the last patient. Reader confidence increased in

32 of 49 studies (65.3%) for both readers, with consistently

high confidence (scores of 4 or 5) after SPECT/CT review.

Although the low-dose CT portion of the study was

primarily used for lesion localization and attenuation correc-

tion, the majority of lesions had corresponding anatomic find-

ings, which improved both the accuracy of lesion classification

and reader confidence. Anatomic findings that were indicative

of a physiologic process included fusion of activity to normal

294

gallbladder, liver, spleen, kidneys, thyroid, abdominal wall

skin, and bowel, including demonstration of splenules in

two cases, which may otherwise have been misdiagnosed as

abdominal disease (nodal metastatic deposits).

Anatomic findings suggestive of somatostatin-expressing

neoplasms included soft-tissue masses, lung nodules, mucosal

bowel thickening, central hepatic tumor necrosis, desmoplas-

tic reactions (carcinoid), lymphadenopathy, and lytic bone

lesions, whereas active inflammatory processes were suggested

TABLE 1. Incremental Diagnostic Value of SPECT/CT Imaging, Impact on Patient Management, and Anatomic Findings

Change in Management

Patient Diagnosis SPECT/CT Region Reader 1 Reader 2

Incremental Value

of SPECT/CT Imaging

Anatomic Findings

on CT Imaging

2 Paraganglioma Abdomen, Thorax Minor* Majory R1 mesenteric

Dx / para-aortic Dx

R2 bowel N / para-

aortic Dx

Lung nodules,

pancreatic mass,

para-aortic LN

5 Glucagonoma Abdomen Nonez Major R2 liver Dx / gallbladder N

R2 bowel Dx / splenule

Gallbladder, splenule

9 Gastrinoma Abdomen Minor Minor R1, R2 pancreatic

Dx / mesenteric Dx

Splenule, mesenteric LN,

bowel N

10 EPT Abdomen Major Major R1 diagnosed

pancreatic and gastric Dx

R2 mesenteric

Dx / pancreatic

and gastric Dx

Gastric wall

thickening, pancreatic mass

11 Paraganglioma Abdomen, Thorax Minor Minor R1, R2 superior

localization of multiple

foci

Multiple bone lesions

(humeri, ribs, thoracic spine,

pelvic)

Liver lesion

13 Gastrinoma Abdomen Major Major R1, R2 liver

Dx / duodenum N

Duodenum N

14 Carcinoid Abdomen Minor None R1 mesenteric

Dx / small-bowel Dx

Small-bowel mass

15 Carcinoid Abdomen None Major R2 suprapubic

Dx / bowel N

Suprapubic bowel N

16 EPT Abdomen, Thorax Minor Minor R1, R2 thyroid N Mediastinal and para-aortic

LN, thyroid N

18 NET Head and neck

Abdomen

Minor Minor R1 diagnosed

maxillary sinus Dx

Auricular Dx / mastoid

airspace Dx Diagnosed

mediastinal Dx

R2 diagnosed

maxillary sinus Dx

Diagnosed mastoid

airspace Dx

Supraclavicular muscle

N / mediastinal Dx

Mastoid airspace

opacification

Maxillary sinus

opacification, mediastinal

adenopathy

20 Carcinoid Abdomen Major Major R1 diagnosed

liver and mesenteric Dx

R2 diagnosed liver Dx

Liver lesion,

mesenteric mass

21 MTC Abdomen, Thorax Major Minor R1 diagnosed

humeral Dx

R2 localization

of humeral Dx

Humeral bone

lesion,

thyroid N

22 Carcinoid Abdomen Major None R1 diagnosed liver Dx Liver lesion,

pancreatic mass

23 MTC Abdomen Minor Major R1 localized

thoracic Dx

R2 diagnosed

thoracic Dx

Right upper

lobe lung infiltrate,

probably in external-beam

radiation field

33 EPT Abdomen None Minor R2 pancreatic

Dx / portocaval Dx

Portocaval LN

34 Carcinoid Abdomen Major None R1 diagnosed

pancreatic Dx

Pancreatic mass

(continued on next page)


295

TABLE 1. (continued) Incremental Diagnostic Value of SPECT/CT Imaging, Impact on Patient Management, and AnatomicFindings

Change in Management

Patient Diagnosis SPECT/CT Region Reader 1 Reader 2

Incremental Value

of SPECT/CT Imaging

Anatomic Findings

on CT Imaging


adrenal Dx

Adrenal mass

37 Carcinoid Abdomen, Thorax Major None R1 diagnosed

adrenal Dx

Adrenal mass,

gastric wall thickening

38 Carcinoid Abdomen, Thorax Minor Minor R1, R2 abdominal Dx /

pancreatic Dx

Pancreatic mass


pelvic Dx

Pelvic mass,

liver lesions, pancreatic

mass

42 MEN type I Abdomen Major None R1 diagnosed

superficial skin

contamination

Abdominal wall skin N

43 Carcinoid Abdomen Major None R1 liver

Dx / gallbladder N

Gallbladder N

44 EPT Abdomen Major None R1 diagnosed

pancreatic Dx

Pancreatic mass

Dx, disease; EPT, endopancreatic tumor; LN, lymph node; MEN, multiple endocrine neoplasia; MTC, medullary thyroid carcinoma; N, normal

(physiologic); NET, neuroendocrine tumor; R1, reader 1 interpretation; R2, reader 2 interpretation; SPECT, single photon-emission computed

tomographic; CT, computed tomographic.

*SPECT/CT change in lesion location or characterization unlikely to be clinically significant.ySPECT/CT change in lesion location and/or characterization likely to significantly affect patient management.zSPECT/CT imaging did not change lesion location or characterization over planar and SPECT imaging.


by activity present at surgical and tracheotomy sites, pulmo-

nary airspace opacities, or external beam irradiation sites.

Histologic confirmation of SRS reports was obtained in 12

of 49 patients, imaging correlation of abnormal findings on

CT imaging or magnetic resonance imaging in 27 of 49

patients, and negative findings corroborated on CT imaging

or magnetic resonance imaging in 14 of 49 patients. In four

patients, progress somatostatin receptor scintigraphy was the

only follow-up imaging modality. Validation of scan interpre-

tation was not performed in a further four patients, apart from

clinical follow-up to 12 months.

DISCUSSION

In parallel with the increasing use of hybrid 2- [18F]fluoro-

deoxyglucose positron emission tomographic/CT cameras

for oncology imaging, there is growing interest in the role

and benefits of hybrid gamma cameras with inline low-dose

CT imaging, primarily for the purposes of localization and

attenuation correction. Such integrated SPECT/CT systems

provide an efficient method for the accurate registration of

functional and anatomic images and should thus appeal to

readers of functional images having relatively coarse spatial

resolution and a paucity of recognizable anatomic informa-

tion. However, the clinical role of fusion imaging, including

indications for its use and whether it provides any additional

296

benefit over protocols using separate planar and SPECT

SRS imaging and diagnostic-quality CT imaging, remains

to be determined.

Indications for SPECT/CT imaging in our series

included the accurate localization of focal activity seen on

planar and SPECT imaging, the assessment of low-grade

head and neck or thoracic activity, evaluation for local recur-

rence at a surgical site, the evaluation of a mass on diagnostic

CT imaging, and the assessment of suspected physiologic

abdominal activity with atypical appearance. We found

that the additional diagnostic information derived

from 111In pentetreotide SPECT/CT imaging over conven-

tional planar and SPECT imaging provides superior lesion

localization and characterization and increased reader confi-

dence. This information was considered very likely to influ-

ence management decisions by diagnosis of sites of disease,

allowing more precise organ localization of disease, which

could alter surgical planning, and by confirming physiologic

uptake, thereby avoiding false-positive studies. This was

achieved with a modest additional radiation exposure to

each patient of 2 to 4 mSv on average, although the minority

of patients required SPECT/CT imaging of two regions of

interest, with consequent higher radiation dose. On the basis

of these findings, we have changed our department protocol

to include routine SPECT/CT imaging for the evaluation

of NETs with somatostatin receptor scintigraphy.


Clinical studies addressing the diagnostic value of SRS

SPECT/CT imaging have been reported (7–15). Perri et al

(9) found that SRS SPECT/CT imaging correctly classified

lesions in a higher proportion of patients than SRS SPECT

imaging (75 of 81 [92.6%] vs 64 of 81 [79%]), including accu-

rate localization in 160 of 169 lesions (94.7%). Krausz et al (10)

found that SPECT/CT imaging provided additional diagnostic

value in 23 of 72 patients and changed management in 10 of 72

patients. Although SPECT/CT imaging provided no addi-

tional value in the 28 studies with negative results among the

72 patients, it did improve reader confidence in such studies.

Pfannenberg et al (11) found in a mixed cohort of 50

patients with NETs that 111In octreotide/131I meta-iodoben-

zylguanidine SPECT/CT imaging had sensitivity of 92% and

specificity of 87% compared to diagnostic-quality CT

imaging, which had sensitivity of 92% and specificity of

21%. Gabriel et al (12), in a group of 53 patients, found sensi-

tivity of 95% and specificity of 100% for 99mTc octreotide

SPECT/CT imaging, which compared favorably to planar

and SPECT imaging, with sensitivity of 64% and specificity

of 64%, and diagnostic-quality CT imaging, with sensitivity

of 82% and specificity of 68%. Amthauer et al (13), in 29

patients, compared hybrid SPECT/CT fusion to retrospective

software fusion and side-by-side interpretation of 111In

octreotide SPECT imaging and diagnostic-quality CT

imaging, divided into different body regions (thorax, skel-

eton, abdomen, and rectum). They found that the registration

of anatomic and functional images obtained with an inte-

grated SPECT/CT system compared favorably with that

obtained by retrospective (ie, software) methods and was far

faster than such methods. However, for the latter methods,

the diagnostic-quality CT imaging did provide additional

diagnostic information over that provided by the low-dose

CT imaging used for anatomic localization.

In a smaller study with 29 patients consisting primarily of

biopsy-proven carcinoid tumors, Hillel et al (14) found that

in 15 of 29 studies with abnormal results, SPECT/CT

imaging improved diagnoses in 11 cases and changed manage-

ment in 7 cases. The ability of CTattenuation-corrected SRS

SPECT imaging to increase the intensity and contrast of more

centrally located foci was shown in a group of 17 patients by

Ruf et al (6).

We recognize several limitations to this study. The heter-

ogenous patient population, with only small representative

numbers in each group, and the inability to histologically

confirm all sites of disease meant that we could not assess

diagnostic test performance for SRS SPECT/CT imaging

in our study (ie, sensitivity, specificity, and accuracy). The

definitions of major and minor impacts on patient manage-

ment are subjective and depend in part on the overall disease

burden of each patient. Therefore, the identification of

disease on SPECT/CT imaging as a solitary site was consid-

ered major, whereas in a patient with widespread metastases,

an additional site was considered to have minor or no

impact on management. Our study did not address the

performance of SPECT/CT imaging in comparison to

either diagnostic CT imaging alone or planar and SPECT

imaging with side-by-side visualization of diagnostic CT

imaging. This would be relevant for centers wishing to

perform the CT component of the SPECT/CT study as

diagnostic quality with contrast and would be a subject of

interest for future study.

CONCLUSION

Hybrid 111In pentetreotide SPECT/CT imaging provides

incremental diagnostic value and greater reader confidence

over planar and SPECT imaging in a significant proportion

of patients when used in diagnostically problematic cases.

This is achieved though superior lesion localization, the iden-

tification of physiologic activity, and additional anatomic

information derived from the nondiagnostic CT portion of

the study.

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incremental value of 111-in pentetreotide spect/ct fusion imaging of neuroendocrine tumors

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