Role of 18F-fluorodeoxyglucose positron emission tomography in preoperative assessment of cytologically indeterminate thyroid nodules.

Abstract

The objective of the study was to determine the diagnostic accuracy of (18)F-fluorodeoxyglucose ((18)F-FDG) positron emission tomography (PET) in the preoperative diagnosis of thyroid nodules with indeterminate fine-needle aspiration biopsy results.
Forty-two consecutive patients with thyroid nodules with indeterminate cytological results participated in this study. Abnormal (18)F-FDG PET uptake was assessed visually and by measuring the maximum standardized uptake value (SUVmax) in thyroid topography. All these results were compared with the final pathological results.
The presence of focal uptake correlated with a greater risk of malignancy (P = 0.018). All 11 malignant nodules had focal uptake (sensitivity of 100%). Of the 31 patients with benign nodules, there were 19 with positive uptake (specificity of 38.7%). The pre-PET probability of cancer was 26.2% (11 of 42), and this probability increased to 36.7% after PET for those patients whose exam showed focal uptake (11 of 30). The preoperative use of (18)F-FDG PET would result in a significant reduction (39%, 12 of 31) in the number of thyroidectomies performed in patients with benign lesions. SUVmax could not improve this degree of accuracy. There was no correlation between thyroid nodule size and SUVmax value (P = 0.96). Patients with carcinomas were younger than patients with benign lesions (P = 0.048). There was no other clinical, laboratory, or ultrasonographic variable related to malignancy.
(18)F-FDG PET provides high sensitivity to malignant lesions and may be a potentially useful tool in the evaluation of thyroid nodules with indeterminate cytological findings. For these nodules the number of unnecessary thyroidectomies in a hypothetical algorithm using (18)F-FDG PET would be reduced by 39%.

Full text

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BRIEF REPORT
Role of18F-Fluorodeoxyglucose Positron Emission
Tomography in Preoperative Assessment of Cytologically
Indeterminate Thyroid Nodules
Fernando M. Sebastianes, Juliano J. Cerci, Patricia H. Zanoni, Jose ´ Soares, Jr., Lilian K. Chibana,
Eduardo K. Tomimori, Rosalinda Y. A. de Camargo, Marisa Izaki, Maria Clementina P. Giorgi,
Jose ´ Eluf-Neto, Jose ´ Cla ´udio Meneghetti, and Maria Adelaide A. Pereira
Divisions of Endocrinology (F.M.S., P.H.Z., E.K.T., R.Y.A.d.C., M.A.A.P.) and Nuclear Medicine (J.J.C., J.S., L.K.C., M.I.,
M.C.P.G., J.C.M.), Hospital das Clı ´nicas da Faculdade de Medicina da Universidade de Sa ˜o Paulo, CEP 05403-000 Sa ˜o
Paulo, Brazil; and Department of Preventive Medicine (J.E.-N.), Faculdade de Medicina da Universidade de Sa ˜o Paulo,
CEP 01246-903 Sa ˜o Paulo, Brazil
Objective:Theobjectiveofthestudywastodeterminethediagnostic
accuracy of18F-fluorodeoxyglucose (18F-FDG) positron emission to-
mography(PET)inthepreoperativediagnosisofthyroidnoduleswith
indeterminate fine-needle aspiration biopsy results.
Methods: Forty-two consecutive patients with thyroid nodules with
indeterminate cytological results participated in this study. Abnor-
mal18F-FDGPETuptakewasassessedvisuallyandbymeasuringthe
maximum standardized uptake value (SUVmax) in thyroid topogra-
phy. All these results were compared with the final pathological
results.
Results: The presence of focal uptake correlated with a greater risk
of malignancy (P ? 0.018). All 11 malignant nodules had focal uptake
(sensitivity of 100%). Of the 31 patients with benign nodules, there
were 19 with positive uptake (specificity of 38.7%). The pre-PET
probability of cancer was 26.2% (11 of 42), and this probability in-
creased to 36.7% after PET for those patients whose exam showed
focal uptake (11 of 30). The preoperative use of18F-FDG PET would
result in a significant reduction (39%, 12 of 31) in the number of
thyroidectomies performed in patients with benign lesions. SUVmax
could not improve this degree of accuracy. There was no correlation
between thyroid nodule size and SUVmax value (P ? 0.96). Patients
with carcinomas were younger than patients with benign lesions (P ?
0.048). There was no other clinical, laboratory, or ultrasonographic
variable related to malignancy.
Conclusions:18F-FDG PET provides high sensitivity to malignant
lesions and may be a potentially useful tool in the evaluation of
thyroid nodules with indeterminate cytological findings. For these
nodules the number of unnecessary thyroidectomies in a hypothetical
algorithm using18F-FDG PET would be reduced by 39%. (J Clin
Endocrinol Metab 92: 4485–4488, 2007)
18F
appropriate for differential diagnosis of benign and malig-
nant lesions in the preoperative evaluation of thyroid nod-
ules cytologically diagnosed as follicular neoplasm (1, 2).
However, a recent study has challenged the degree of accu-
racy of18F-FDG PET for this application (3). The aim of this
prospective study was to determine the diagnostic accuracy
of
nodules with indeterminate cytological results and the po-
tential of18F-FDG PET for reducing the number of thyroid-
ectomies performed on nodules that subsequently proved to
be benign.
-FLUORODEOXYGLUCOSE (18F-FDG) positron emis-
sion tomography (PET) has been suggested as a tool
18F-FDG PET in the preoperative diagnosis of thyroid
Subjects and Methods
Subjects
In a university hospital in Brazil, 42 patients (38 female) with inde-
terminate cytological results underwent hemithyroidectomy or total
thyroidectomyandhadtheir18F-FDGPETfindingscomparedwiththeir
histopathological results (Table 1). Incidentally found papillary micro-
carcinomas were not included in the analysis. Exclusion criteria were
uncontrolled diabetes mellitus, other known malignancies, pregnancy,
and abnormal TSH levels. The study was approved by the Ethical Board
of the Clinical Hospital of Sa ˜o Paulo University, and written informed
consent was obtained from all patients.
Fine-needle aspiration biopsy was performed by an experienced cy-
topathologist, and all aspirates were stained with Papanicolaou staining
and reviewed by two cytopathologists. Cytologically indeterminate pat-
terncompriseshypercellularfollicularandoxyphilicnodulessuggestive
of follicular neoplasm and also includes lesions that are suspect but not
diagnostic of papillary carcinoma (4). The criteria used for histopatho-
logical diagnosis of benign vs. malignant diseases were based on the
histological classification of thyroid tumors by the Word Health Orga-
nization (5).
The mean age was 45.3 ? 16.3 yr (range 18–80 yr). All patients
underwent thyroid ultrasonography, 50% of them having just one nod-
ule. The nodules had a mean maximum diameter in histopathological
exam of 3.0 ? 1.8 cm (range 0.4–8.5 cm). The interval between fine-
needle aspiration biopsy and18F-FDG PET was at least 17 d.
First Published Online August 7, 2007
Abbreviations:18F-FDG,18F-fluorodeoxyglucose;PET,positronemis-
sion tomography; ROI, region of interest; SUVmax, maximum standard
uptake value.
JCEM is published monthly by The Endocrine Society (http://www.
endo-society.org), the foremost professional society serving the en-
docrine community.
0021-972X/07/$15.00/0
Printed in U.S.A.
The Journal of Clinical Endocrinology & Metabolism 92(11):4485–4488
Copyright © 2007 by The Endocrine Society
doi: 10.1210/jc.2007-1043
4485

Page 2

18F-FDG PET imaging
All patients fasted for at least 6 h. Their fasting glucose level was less
than 160 mg/dl. PET imaging acquisition started after a 60-min uptake
period after iv administration of 296–444 MBq (8–12 mCi) of18F-FDG.
The patients were instructed to rest comfortably between injection and
scanning. Images in two dimensions were captured by a GE Advance
PET scanner (General Electric Medical Systems Advance, Milwaukee,
WI). High-resolution images were taken with attenuation correction in
two or three bed positions, from the base of the skull to the middle
thorax.
PET images were displayed as projections and in transaxial, coronal,
and sagittal tomographic sections. Visual inspection of the images was
performed independently by two experienced observers. These observ-
ers were not aware of the location of the nodule, ultrasonography, and
histopathological examination.18F-FDG PET-positive results were de-
finedasthepresenceofanyfocal18F-FDGuptakeinthyroidtopography,
standing out from the thyroid bed background. There was 100% agree-
ment between the two observers who analyzed these results.
Regions of interest (ROIs) were selected for quantification of18F-FDG
uptake from the visible lesions. When the thyroid nodule could not be
seen,largeROIsthatincludedthethyroiditselfwereselected.Maximum
standard uptake values (SUVmax) were calculated.
Statistical analysis
A computer program (SPSS for Windows, version 13.0; SPSS Inc.,
Chicago, IL) was used for two-tailed statistical analysis. The level of
significance was set at 0.05. Correlations were determined using the
Spearman test. Analyses were also carried out using the Mann-Whitney
test, independent samples t test, and Fisher’s exact test, where appro-
priate, as shown in Results.
Results
Final pathological diagnoses revealed 11 well-differenti-
ated thyroid carcinomas (26.2%), 22 adenomatous goiters
(52.4%), eight follicular adenomas (19.0%), and one thyroid-
itis (2.4%) (Table 1). Of the 11 patients with well-differenti-
TABLE 1. Clinical and ultrasonographic characteristics of patients and their histopathological and PET results
No.Age (yr)/sex
Ultrasonographic
characteristics
Solid hypoechogenic
Solid hypoechogenic
Solid isoechogenic
Solid hypoechogenic
Solid-cystic nodule
Solid isoechogenic
Solid hypoechogenic
Solid-cystic nodule
Solid isoechogenic
Solid isoechogenic
Solid hypoechogenic
Solid-cystic nodule
Solid-cystic nodule
Solid-cystic nodule
Solid hyperechogenic
Solid-cystic nodule
Solid hypoechogenic
Solid isoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid multinodular
Solid-cystic multin
Solid-cystic nodule
Solid isoechogenic
Solid-cystic nodule
Solid hypoechogenic
Solid-cystic nodule
Solid-cystic nodule
Solid hypoechogenic
Solid hypoechogenic
Solid isoechogenic
Solid-cystic nodule
Solid hypoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid hypoechogenic
Solid-cystic nodule
Solid hypoechogenic
Solid hypoechogenic
Histopathological
diagnosis
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Follicular adenoma
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Follicular adenoma
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Classic V papillary carc
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Follicular adenoma
Follicular carcinoma
Follicular V papillary carc
Adenomatous goiter
Adenomatous goiter
Adenomatous goiter
Clear cell V papillary carc
WD carcinoma NOS
Follicular V papillary carc
Follicular V papillary carc
Follicular carcinoma
Adenomatous goiter
Follicular adenoma
Follicular adenoma
Adenomatous goiter
Follicular V papillary carc
Adenomatous goiter
Follicular adenoma
Classic V papillary carc
Hashimoto’s thyroiditis
Oxyphilic cell adenoma
Classic papillary carc
Adenomatous goiter
Follicular adenoma
Nodule max
diameter (cm)a
1.3
5.4
2.6
3.5
2.3
3.0
1.5
1.5
2.4
2.0
1.5
4.8
3.5
3.0
1.5
3.0
3.0
3.5
0.9
3.0
4.0
4.0
4.5
1.0
2.0
8.5
7.0
2.0
3.5
3.5
2.0
1.5
3.3
3.4
2.5
2.5
0.4
1.9
1.1
8.0
1.3
4.5
PETSUVmax
1
2
3
4
5
6
7
8
9
80/F
74/M
22/F
66/F
51/F
38/F
66/F
51/F
18/F
22/F
51/F
37/F
49/F
46/F
50/F
64/F
43/F
47/F
23/M
30/F
53/F
63/F
42/F
48/F
27/M
21/F
26/F
32/F
39/F
71/F
39/F
38/F
30/F
25/F
56/F
30/F
43/F
65/F
55/F
65/F
44/F
61/M
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
0
0
0
1.7
1.8
1.8
1.9
2.4
2.4
2.7
3.5
3.7
3.8
3.8
3.9
4.0
4.1
4.5
5.4
5.4
5.5
5.8
5.8
5.9
6.3
7.1
7.4
7.8
8.8
9.8
9.9
10.2
10.8
10.9
12.5
13.0
14.9
16.1
21.7
46.5
62.6
77.5
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
Patients 8, 15, and 40 had indeterminate cytological results with oxyphilic cells. Patient 7 had two nodules with indeterminate cytological
results (both were adenomatous nodules and both were FDG negative), and only the larger one was included in the analysis. Patient 37 was
recommendedforthyroidectomybecausethenodulewashighlysuspectwhensubjectedtoDopplerultrasonography.M,Male;F,female;Multin,
multinodular; Carc, carcinoma; V, variant; WD, well differentiated; NOS, not otherwise specified.
aAccording to histopathological exam.
4486
J Clin Endocrinol Metab, November 2007, 92(11):4485–4488Sebastianes et al. • PET for Thyroid Nodule Diagnosis

Page 3

ated thyroid carcinomas, eight had papillary, two had fol-
licular, and one had a well-differentiated thyroid carcinoma
nototherwisespecified.Thepresenceoffocalthyroiduptake
was associated with increased risk of malignancy (Fisher’s
exacttest,P?0.018).Allmalignantnoduleshadfocaluptake
(sensitivity of 100%). Of the 31 patients with benign nodules,
12 (39%) had negative uptake (Table 2). The pre-PET prob-
ability of cancer of 26% (11 of 42) rose to 37% (11 of 30) after
PET. SUVmax levels were not significantly greater in ma-
lignant than benign thyroid nodules (Mann-Whitney test,
P ? 0.069) and could not improve the accuracy of18F-FDG
PET beyond that obtained by the analysis of focal uptake
presence. All nodules without18F-FDG focal uptake had a
level of SUVmax of less than 3.7, except one patient with a
diffusethyroid18F-FDGuptake,butnofocaluptake,thathad
a level of SUVmax of 3.9.
Although the mean maximum diameter of the malignant
thyroid nodules (4.1 ? 2.6 cm) was greater than that of the
benign nodules (2.6 ? 1.2 cm), this difference was not con-
sidered to be statistically significant (t test, P ? 0.10). There
wasnocorrelationinsizeofthyroidnoduletoSUVmaxvalue
(Spearman, P ? 0.96). Regarding the benign nodules, size
was not associated with the SUVmax value (Spearman, P ?
0.57) nor the presence of focal uptake in18F-FDG PET (t test,
P ? 0.41). Of the clinical, laboratory, and ultrasonography
parameters, the only one that was associated with malig-
nancy was age. The mean age of patients with thyroid car-
cinomas was 37 ? 13.6 yr, lower than patients with benign
lesions, whose mean age was 48.2 ? 16.3 yr (t test, P ? 0.048).
Age, however, was not associated with either SUVmax
value (Spearman, P ? 0.70) or presence of focal uptake
(t test, P ? 0.34).
Four patients with benign thyroid lesions and positive
18F-FDG PET had incidental papillary microcarcinomas in
the same lobe (maximum diameters of 0.5, 0.5, 0.2, and 0.1
cm). All these cases were considered as false-positive results
by the analysis. Unexpected additional findings were found
in two of the 42 patients (4.8%): absence of18F-FDG uptake
in one lobe of the cerebellum (a cystic neoplasia in computed
tomography)inpatientnumber11(Table1)andfocaluptake
in mediastinum in patient number 1 (the thorax computed
tomography with iv contrast was normal).
Discussion
Our results confirm the findings of several studies (1–3,
6–11) that suggest that18F-FDG PET may have a very high
negative predictive value for detecting malignancy in the
preoperative evaluation of thyroid nodules (Table 2). From
more than 100 patients with malignant thyroid nodules eval-
uated in the literature, the only reported false-negative re-
sults are one case in a study that did not use a modern PET
camera (9) and seven nodules from the study by Mitchell et
al. (12), five being incidental microcarcinomas, one a papil-
lary carcinoma measuring 3.5 cm ? 2.6 cm in diameter
(SUVmax of 2.3), and one a renal carcinoma metastatic to
thyroid(SUVmaxof2.3).Thisstudy,donebyPET-computed
tomography, was the only one that included incidental mi-
crocarcinomas in the analysis. Of note, if the diagnostic cri-
teria adopted by Mitchell et al. were to be changed from an
SUVmax greater than 5.0 to an SUVmax greater than 0 (im-
plying some degree of nodule uptake), then the two major
carcinomas would have to be considered true-positive re-
sults, although the specificity among thyroid nodules with
indeterminate cytological results would be considerably re-
duced (Table 2).
In our study, 39% of the patients with benign thyroid
noduleshadnofocal18F-FDGuptake.Othersignificantstud-
ies in literature had variable results (Table 2). In studies by
Kresnik et al. (2) and De Geus-Oei et al. (1), 56 and 66%,
respectively,ofthepatientswithbenignnoduleshadnofocal
FDGuptakewhen18F-FDGPETwasusedinthepreoperative
evaluationofthyroidnoduleswithindeterminatecytological
results. It should be emphasized, however, that in the study
by Kresnik et al. (2), patients were from an iodine-poor area,
and that in the study from De Geus-Oei (1), only patients
with palpable thyroid nodules were selected and that their
size and ultrasonographic characteristics were not reported.
On the other hand, in the study by Kim et al. (3), all benign
thyroid nodules were18F-FDG avid and the only character-
istic associated with SUVmax value was nodule size. In our
study, however, the maximum nodule diameter was not
related to SUVmax value or focal uptake presence in the
thyroidbed.Neitherwasanyrelationshipapparentwhenthe
subgroup of benign and malignant thyroid nodules was
analyzed.
The reasons for these differences are unclear and may be
related to a different pattern of gene expression between
benign nodules in different regions of the world because
malignant nodules are consistently FDG avid in all studies.
Variations in technique and selection of patients could also
be a reason. Prior studies reported increased glucose trans-
porter-1 protein immunostaining (13) and gene expression
TABLE 2. Summaries of the main studies assessing18F-FDG PET in preoperative evaluation of indeterminate thyroid nodules
Source
No. of surgical
patients
37
Diagnostic criteria
(in thyroid bed)
SUVmax ? 2.0
Positive FU
SUVmax ? 5.0
Positive NU
Positive FU
Positive FU
Positive FU
Percentage of
true-negative results
63 (17 of 27 patients)
56 (15 of 27 patients)
91 (21 of 23 nodules)
39 (9 of 23 nodules)
66 (25 of 38 patients)
0 (0 of 21 patients)
39 (12 of 31 patients)
Percentage of
false-negative results
0 (10 patients)Kresnik et al. (2)
Mitchell et al. (12)a
24b
100 (1 of 1 nodule)c
0 (0 of 1 nodule)c
0 (6 patients, 7 nodules)
0 (15 patients)
0 (11 patients)
De Geus-Oei et al. (1)
Kim et al. (3)
This study
FU, Focal uptake; NU, nodule uptake (defined as an SUVmax ? 0).
aThis study used18F-FDG PET-CT instead of18F-FDG PET-scan.
bThis is the number of thyroid nodules evaluated; it is not clearly stated how many of these nodules were present in the same patient.
cThis nodule was a papillary cancer measuring 3.5 ? 2.6 cm with an SUVmax of 2.3.
44
36
42
Sebastianes et al. • PET for Thyroid Nodule DiagnosisJ Clin Endocrinol Metab, November 2007, 92(11):4485–4488
4487

Page 4

(14) in thyroid cancer in relation to benign lesions, support-
ing the view that18F-FDG PET may be a useful tool when
evaluating thyroid nodules.
OurdataalsosupporttheviewintroducedbyDeGeus-Oei
(1) that focal uptake presence should be the cornerstone in
any analysis of18F-FDG PET used in the evaluation of thy-
roid nodules, as shown in Table 2, although the specificity
of our findings in our study was only 39%. The value of
SUVmax depends on acquisition, reconstruction and ROI
parametersandtheparticularPETscannerusedfortheexam
(1,15).Thisintroducesmanyfactorsthatmayleadtopossible
biasintheSUVmaxmeasurementmakingitdifficulttoapply
in different centers. This may explain the different cutoffs of
SUV found in different studies (1, 2, 12).
The finding in our study of a patient with negative thyroid
focal uptake in a benign lesion but with an SUVmax of 3.9
(?3.7) was probably due to the coexistence of lymphocytic
thyroiditis resulting in diffuse thyroid uptake in18F-FDG
PET (16). However, even in patients in whom thyroiditis
coexists, it may be appropriate to recommend18F-FDG PET
because nine of the 11 patients with lymphocytic thyroiditis
in histopathological examinations did not show an alteration
in18F-FDGPETsufficientlysignificanttoimpairtheaccuracy
of this exam.
Finally, papillary carcinoma was the malignancy most fre-
quently diagnosed in our study. This may be related to the
elevated daily ingestion of iodine that is common in Brazil
(17, 18), which could be responsible for substantially low-
ering the incidence of follicular as opposed to papillary thy-
roid carcinomas (19, 20).
In conclusion,18F-FDG PET provides a high negative pre-
dictive value in the preoperative evaluation of thyroid ma-
lignancyinnoduleswhosecytologicalresultisindeterminate
butapositivepredictiverateofonly37%.Ifweconsiderhigh
sensitivity to be the most important characteristic of a test
designed to determine which patients with indeterminate
cytological findings should undergo surgery, then18F-FDG
PET can be a useful tool in the evaluation of these nodules.
For these nodules the number of unnecessary hemithyroid-
ectomies in a hypothetical algorithm using
would be reduced by 39%.
18F-FDG PET
Acknowledgments
We thank the staff from the Divisions of Endocrinology, Head and
Neck Surgery and Nuclear Medicine from Hospital das Clinicas da
Faculdade de Medicina da USP, Sa ˜o Paulo, Brazil, for their professional
assistance. We also thank Alexander A. de Lima Jorge for his sugges-
tions.
Received May 10, 2007. Accepted July 31, 2007.
Address all correspondence and requests for reprints to: Maria Ad-
elaide Albergaria Pereira, M.D., Division of Endocrinology and Metab-
olism, Hospital das Clı ´nicas, University of Sa ˜o Paulo Medical School,
AvenidaDrEne ´asdeCarvalhoAguiar,255,7thfloor,CEP05403-000Sa ˜o
Paulo (SP), Brazil.
Disclosure Statement: The authors have no conflict of interest.
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JCEM is published monthly by The Endocrine Society (http://www.endo-society.org), the foremost professional society serving the
endocrine community.
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