Ann Surg Oncol (2011) 18:1306–1311

DOI 10.1245/s10434-010-1469-2

ORIGINAL ARTICLE – ENDOCRINE TUMORS

Characteristics of Primary Papillary Thyroid Carcinoma

with False-Negative Findings on Initial 18F-FDG PET/CT
Jin Woong Choi, MD1, Young Hoon Yoon, MD1, Yeo Hoon Yoon, MD1, Seong Min Kim, MD2,
and Bon Seok Koo, MD1

1
Department of Otolaryngology-Head and Neck Surgery, Cancer Research Institute, Research Institute for Medical
Sciences, Chungnam National University College of Medicine, School of Medicine, Daejeon, Korea; 2Department of
Nuclear Medicine, Chungnam National University College of Medicine, Daejeon, Korea

ABSTRACT there were no significant differences between 18F-FDG

Background. We often observe that uptake of tracer is not
detected in the primary cancer focus in patients with his-
tologically proven papillary thyroid carcinoma (PTC) on
preoperative 18F-fluorodeoxyglucose positron emission
tomography-computed tomography (18F-FDG PET/CT).
Therefore, we analyzed the clinical and pathologic vari-
ables affecting false-negative findings in primary tumors
on preoperative 18F-FDG PET/CT.
Methods. We retrospectively reviewed the medical
records of 115 consecutive patients who underwent 18F-
FDG PET/CT for initial evaluation and were diagnosed
with PTC by postoperative permanent biopsy. The clinical
and pathologic characteristics that influence the 18F-FDG
PET/CT findings in these patients were analyzed with
respect to the following variables: age, gender, tumor size,
multifocality of the primary tumor, perithyroidal invasion,
lymphovascular or capsular invasion, and central lymph
node metastasis-based final pathology.
Results. Twenty-six (22.6%) patients had false-negative
18
F-FDG PET/CT findings. In patients with negative 18F-
FDG PET/CT findings, tumor size, and perithyroidal and
lymphovascular invasion were significantly less than in
patients with positive 18F-FDG PET/CT findings. Tumors
[1 cm in size were correlated with 18F-FDG PET/CT
positivity. On multivariate analysis, perithyroidal invasion
(P = 0.026, odds ratio = 7.714) and lymphovascular
invasion (P = 0.036, odds ratio = 3.500) were indepen-
dent factors for 18F-FDG PET/CT positivity. However,
Ó Society of Surgical Oncology 2010
First Received: 3 September 2010;
Published Online: 8 December 2010
B. S. Koo, MD
e-mail: bskoo515@cnuh.co.kr
PET/CT positivity and age, gender, capsular invasion, and
central lymph node metastasis based on final pathology.
Conclusions. Tumor size and perithyroidal and lympho-
vascular invasion of papillary carcinoma can influence 18F-
FDG PET/CT findings. Absence of perithyroidal and
lymphovascular invasion were independent variables for
false-negative findings on initial 18F-FDG PET/CT in
patients with PTC.
18
F-Fluorodeoxyglucose positron emission tomography-
computed tomography (18F-FDG PET/CT) is used widely
in diagnosis or preoperative staging of various cancers.1
Furthermore, the integrated PET/CT system makes it pos-
sible to fuse anatomic images with functional images,
which results in better anatomic localization and an
improvement of diagnostic accuracy.2,3 Many studies have
reported the usefulness of 18F-FDG PET/CT in thyroid
cancer. Most of these reports have focused on the role of
follow-up 18F-FDG PET/CT in patients with recurrence,
metastasis, or elevated serum thyroglobulin (Tg) and neg-
ative whole-body bone scans (WBSs).4–7 Recently, there
have been reports about the usefulness of 18F-FDG PET/
CT in initial evaluation of thyroid cancer.8,9 We occa-
sionally observe that uptake of tracer in the primary tumor
focus of patients with pre- or postoperative pathologic-
proven papillary thyroid cancer (PTC) is not detected on
initial 18F-FDG PET/CT. The clinicopathologic character-
istics in such patients with PTC with false-negative
findings for primary tumor on 18F-FDG PET/CT are
expected to differ from patients with PTC with true-posi-
tive findings for primary tumor on 18F-FDG PET/CT;
however, there are no studies which have addressed this
issue to date.
 18
Preoperative F-FDG PET/CT in PTC
Therefore, in the present study we determined the clin-
icopathologic differences between patients with PTC who
have false-negative and true-positive findings based on
18
F-FDG PET/CT, and analyzed clinical and pathologic
variables affecting false-negative findings involving pri-
mary tumors based on preoperative 18F-FDG PET/CT.
PATIENTS AND METHODS
We retrospectively reviewed the medical records of 115
consecutive patients with PTC who underwent 18F-FDG
PET/CT for initial evaluation and had histopathologically
proven PTC by postoperative permanent biopsy. All
patients underwent preoperative ultrasonography (US) and
fine-needle aspiration (FNA) cytology of the primary
tumor. 18F-FDG PET/CT was performed after papillary
thyroid carcinoma was diagnosed from fine-needle aspira-
tion cytology in all patients. All patients were treated with
total thyroidectomy with central lymph node dissection in
the Otorhinolaryngology Department of Chungnam
National University Hospital between September 2009 and
May 2010. Patients with other pathologic types of thyroid
malignancies and thyroiditis, including Hashimoto thy-
roiditis, were excluded from this study. The specimens
after surgery were routinely sectioned every 3 mm and
stained with hematoxylin and eosin for histopathologic
examination. All histologic diagnoses were made by one
pathologist according to the recommendations of the World
Health Organization. The study was approved by the local
Institutional Review Board.
18
F-FDG PET images were acquired with a PET scanner
(GE Discovery ST-16; GE Healthcare, Milwaukee, WI,
USA). The patients were required to fast for at least
6 h before 18F-FDG was injected. PET images were
acquired 1 h after intravenous administration of 18F-FDG
(8.14 MBq/kg). PET data were reconstructed using order-
subsets expectation maximization. Data obtained from CT
acquisitions were used for low-noise attenuation correction
of PET emission data and for fusion of attenuation-cor-
rected PET images with corresponding CT images. 18F-
FDG PET/CT was visually analyzed by one experienced
nuclear medicine physician. Focally abnormal 18F-FDG
activity of higher intensity than the surrounding tissues,
which was not related to benign or physiologic 18F-FDG
uptake or was localized in a suspicious mass on CT, was
defined as a positive finding. Tracer uptake was considered
to be a negative finding when equal to or lower than
background activity.
The clinicopathologic differences between PTCs with
false-negative and true-positive findings on 18F-FDG PET/
CT, and the factors affecting false-negative findings for
primary tumors on preoperative 18F-FDG PET/CT, were
1307
analyzed with respect to the following variables: age,
gender, tumor size, multifocality of the primary tumor,
presence of perithyroidal invasion, lymphovascular or
capsular invasion, and presence of central lymph node
metastasis.
SPSS (version 17 software; SPSS Inc., Chicago, IL,
USA) was used for statistical analysis. Several clinico-
pathologic factors potentially associated with false-
negative findings on 18F-FDG PET/CT were addressed
with univariate analysis using Fisher’s exact or v2 tests. A
binary logistic regression test was used for multivariate
analysis of variables that were statistically significant on
univariate analysis. We regarded statistical significance as
P value \0.05.
RESULTS
The 115 study patients consisted of 97 women and 18
men with median age of 49 years (range 21–81 years). The
median size of the primary thyroid cancer was 0.7 cm
(range 0.2–4.2 cm). Multifocal cancer lesions were found
in 52 of the patients (45.2%). Perithyroidal, lymphovas-
cular, and capsular invasion were found in 45 (39.1%), 56
(48.7%), and 62 patients (53.9%), respectively. Central
lymph node metastases were found in 30 patients (26.1%).
Mean serum Tg level was 27.5 ng/ml in the positive
18
F-FDG PET/CT group versus 20.0 ng/ml in the negative
18
F-FDG PET/CT group (Table 1).
Of the 115 patients with PTC, 26 (22.6%) had false-
negative findings on 18F-FDG PET/CT, having pathologic-
proven PTC but not FDG uptake in the primary tumor
focus on 18F-FDG PET/CT preoperatively. In 26 patients
with false-negative findings, the mean size of the primary
papillary carcinoma was 0.5 cm (range 0.3–1.0 cm), and 8
(30.8%) had multifocal primary tumors. Perithyroidal,
lymphovascular, and capsular invasion were found in 3
(11.5%), 5 (19.2%), and 10 patients (38.5%), respectively.
Central lymph node metastases were found in three patients
(11.5%). There were significant difference in primary
tumor size, presence of perithyroidal invasion and lym-
phovascular invasion between patients with PTC who had
false-negative and true-positive findings based on 18F-FDG
PET/CT. However, no significant difference was noted
between the positive and negative 18F-FDG PET/CT
groups in terms of age, gender, presence of multifocality,
capsular invasion or central lymph node metastasis, and
mean serum Tg level (Table 1).
Univariate analysis of potential clinicopathologic factors
associated with false-negative findings on 18F-FDG PET/CT
based on our patients with PTC is shown in Table 2. False-
negative findings on 18F-FDG PET/CT were significantly
more frequent in patients with papillary microcarcinoma
1308 J. W. Choi et al.

TABLE 1 Demographic
Characteristic Positive FDG PET Negative FDG PET Total
characteristics of 115 patients
No. of patients 89 26 115
Age, mean ± SD (years) 49 ± 13 51 ± 8 49 ± 12
Gender (M/F) 11/78 7/19 18/97
Primary tumor size, mean ± SD (cm) 0.94 ± 0.66 0.48 ± 0.22 0.83 ± 0.62
Multifocality (%) 44 (49.4) 8 (30.8) 52 (45.2)
Perithyroidal invasion (%) 42 (47.2) 3 (11.5) 45 (39.1)
Lymphovascular invasion (%) 51 (57.3) 5 (19.2) 56 (48.7)
Capsular invasion (%) 52 (58.4) 10 (38.5) 62 (53.9)
Positive central lymph node (%) 27 (30.3) 3 (11.5) 30 (26.1)
SD Standard deviation, Tg Mean serum Tg level (ng/ml) 27.5 20.0 25.8
thyroglobulin

TABLE 2 Clinicopathologic factors in relation to negative FDG between false-negative results and age, gender, or capsular
PET/CT results in 115 patients with papillary thyroid carcinoma: invasion. Multivariate analysis also revealed that absence of
univariate analysis
perithyroidal (P = 0.047, odds ratio = 3.882) and lym-
Variable Patients with negative FDG P value phovascular invasion (P = 0.028, odds ratio = 3.482) were
PET/CT finding, n (%)
independent variables for false-negative findings on
18
Age (years) F-FDG PET/CT in patients with PTC (Table 3).
\45 5/36 (13.9) 0.131 When we analyzed the data in the subgroup with tumor
C45 21/79 (26.6) size less than 1 cm, false-negative findings on 18F-FDG
Gender PET/CT in this group were significantly more frequent in
Male 7/18 (38.9) 0.120 patients without multifocality, perithyroidal invasion and
Female 19/97 (19.6) lymphovascular invasion (P = 0.035, 0.038, and 0.008,
Tumor size (cm) respectively, Table 4). Multivariate analysis in the sub-
B1.0 25/92 (27.2) 0.019a group revealed that absence of lymphovascular invasion
[1.0 1/23 (4.3) (P = 0.045, odds ratio = 3.486) was the only independent
Multifocality
variable for false-negative findings on 18F-FDG PET/CT
Yes 8/52 (15.4) 0.092
(Table 5).
No 18/63 (28.6)
Perithyroidal invasion
DISCUSSION
a
Yes 3/45 (6.7) 0.001
In the last few years, 18F-FDG PET/CT has been widely
No 23/70 (32.9)
used as a method for diagnosis of various primary, recur-
Lymphovascular invasion
rent, or metastatic cancers.1 With respect to thyroid cancer,
Yes 5/56 (8.9) 0.001a 18
F-FDG PET/CT has been shown to be valuable in
No 21/59 (35.6)
diagnosis of recurrence or metastasis in patients with dif-
Capsular invasion
ferentiated thyroid carcinoma with high Tg levels and
Yes 10/62 (16.1) 0.072
negative WBS findings.4–6,10 Some studies have reported
No 16/53 (30.2)
that preoperative 18F-FDG PET/CT in patients with PTC
Central lymph node metastases
was not useful in detecting the differentiation status of
Yes 3/30 (10.0) 0.055
malignancies and supplementing fine-needle aspiration
No 23/85 (27.1)
biopsy (FNAB) results.7–9 However, other studies have
a
P \ 0.05 between the two categories for a given variable shown that 18F-FDG PET/CT is sensitive in the detection
of patients with PTC with lymph node and distant metas-
(B1 cm) and without perithyroidal invasion and lym- tases.1,6,7 When 18F-FDG PET/CT was used preoperatively
phovascular invasion (P = 0.019, 0.001, and 0.001, for staging of PTC, we occasionally observed that uptake
respectively). False-negative findings on 18F-FDG PET/CT of the tracer in the primary tumor focus was not detected on
were more frequent in patients without central lymph node initial 18F-FDG PET/CT. However, few studies have con-
metastasis than in those with central lymph node metastasis; sidered data on the characteristics of patients with PTC
this result was close to but did not reach statistical signifi- with false-negative findings for primary tumors on
18
cance (P = 0.055). There were no significant differences F-FDG PET/CT. Therefore, we focused on the clinical
 18
Preoperative F-FDG PET/CT in PTC 1309

18
TABLE 3 Multivariate logistic regression for negative F-FDG PET/CT finding
Variables b (SE) P value Exp (b) 95.0% CI Exp(b)
Lower Upper

Tumor size B 1.0 cm 1.100 (1.112) 0.323 3.004 0.340 26.578

No perithyroidal invasion 1.356 (0.684) 0.047 3.882 1.015 14.843
No lymphovascular invasion 1.248 (0.569) 0.028 3.482 1.142 10.618
Constant 0.300 (0.294)
SE Standard error, Exp(b) odds ratio, CI confidence interval

TABLE 4 Clinicopathologic factors in relation to negative FDG and pathologic characteristics associated with false-nega-
PET/CT results in 92 patients with papillary thyroid microcarcinoma: tive findings on preoperative 18F-FDG PET/CT of PTC.
univariate analysis In the current study, tumor size, and perithyroidal
Variable Patients with negative FDG P value and lymphovascular invasion were significantly different
PET/CT finding, n (%) characteristics between patients with PTC with false-neg-
Age (years) ative and true-positive findings on 18F-FDG PET/CT.
\45 5/23 (21.7) 0.596
Microcarcinomas (B1 cm) had more false-negative find-
C45 20/69 (28.9)
ings on 18F-FDG PET/CT than PTCs [1 cm in size. False
negativity occurred in 6.7 and 8.9% of patients with peri-
Gender
thyroidal and lymphovascular invasion, respectively, being
Male 7/15 (46.7) 0.108
significantly less frequent than in patients without peri-
Female 18/77 (23.4)
thyroidal invasion (32.9%) and lymphovascular invasion
Multifocality
(35.6%). Jeong et al.8 showed that 18F-FDG PET/CT
Yes 7/43 (16.3) 0.035a
imaging correlated with tumor size, but was not associated
No 18/49 (36.7)
with extrathyroid invasion in papillary microcarcinoma.
Perithyroidal invasion
Esteva et al.11 reported that tumor size and thyroid capsular
Yes 3/27 (11.1) 0.038a
invasion were significantly associated with positive
No 22/65 (33.8) 18
F-FDG PET/CT findings in diagnosis of recurrence or
Lymphovascular invasion
metastasis in patients with differentiated thyroid cancer. In
Yes 4/36 (11.1) 0.008a
the current study, capsular invasion did not reach signifi-
No 21/56 (37.5) cance (P = 0.072). Central lymph node metastasis was
Capsular invasion closely correlated with 18F-FDG PET/CT results, but was
Yes 10/43 (23.3) 0.487 not statistically significant (P = 0.055).
No 15/49 (30.6) Our study population included many micro-PTC
Central lymph node metastases patients. Some may state that this reflects a patient popu-
Yes 3/17 (17.6) 0.385 lation which is not reflective of those in studies at least in
No 22/75 (29.3) the USA, where diagnostic workup (i.e., FNA) of nodules
a
P \ 0.05 between the two categories for a given variable B1 cm (or B5 mm with suspicious ultrasound findings in a

18
TABLE 5 Multivariate logistic regression for negative F-FDG PET/CT finding in papillary thyroid microcarcinoma subgroup
Variables b (SE) P value Exp (b) 95.0% CI Exp(b)
Lower Upper

No multifocality 0.698 (0.547) 0.201 2.010 0.616 5.471

No perithyroidal invasion 0.925 (0.708) 0.191 2.523 0.941 28.963
No lymphovascular invasion 1.249 (0.622) 0.045 3.486 1.207 16.868
Constant 0.119 (0.334)
SE standard error, Exp(b) odds ratio, CI confidence interval
1310
high-risk group) would not be recommended in the first
place, as proposed in the 2009 revised American Thyroid
Association management guidelines.12 However, according
to the guideline of the National Comprehensive Cancer
Network (NCCN) and the American Association of Clini-
cal Endocrinologists (AACE), the Associazione Medici
Endocrinologi (Italian Association of Clinical Endocrinol-
ogists) (AME), and the European Thyroid Association
(ETA), FNA biopsy is also recommended for nodules of
diameter smaller than 10 mm along with US findings
associated with malignancy, without suggestion of a lower
limit on diameter.13,14 Therefore, we think that FNA of
nodules B1 cm should be considered based on individual
risk factors and US findings.
Because of the partial-volume effect on 18F-FDG PET/
CT imaging, papillary microcarcinomas are difficult to
detect with 18F-FDG PET/CT. Mitchell et al.9 reported that
PTCs [1 cm in size have 18F-FDG PET/CT uptake and
high negative predictive value, although papillary micro-
carcinomas have high false-negative results. In the present
study, papillary microcarcinomas had more false-negative
findings than previously reported.7,9 Tumor size was sta-
tistically significant based on univariate analysis, but was
not significant on multivariate analysis. We therefore think
that, even though tumor size affects 18F-FDG PET/CT
results, tumor size is not an independent factor for
18
F-FDG PET/CT positivity. Nevertheless, further evalua-
tion is needed to identify the factors which contribute to
false-negative 18F-FDG PET/CT findings in terms of pri-
mary tumor size.
Several studies have reported that serum Tg level affects
18
F-FDG PET/CT results.4–7,10,15–17 Menzel et al.16 reported
that 18F-FDG PET/CT is sensitive in patients with Tg level
[1.9 ng/ml in differentiated thyroid cancer. Giammarile
and Schluter15,17 reported that, the higher the serum Tg level,
the more sensitive the 18F-FDG PET/CT result. In the current
study, the mean serum Tg level was 27.5 ng/ml in the posi-
tive 18F-FDG PET/CT group versus 20.0 ng/ml in the
negative 18F-FDG PET/CT group; however, this difference
did not reach significance (P = 0.66). Furthermore, none of
the patients were under thyroid-stimulating hormone (TSH)
stimulated conditions, because all of the patients had
18
F-FDG PET/CT for initial staging of the PTC. Therefore,
we dismissed the effect of serum Tg level on 18F-FDG PET/
CT findings in the present study.
It is well known that age, gender, and histopathologic
characteristics (i.e., tumor size, extrathyroid invasion,
vascular invasion, lymph node metastasis, distant metas-
tasis, and histologic type) are risk factors for aggressive
behavior of well-differentiated thyroid carcinoma.18,19 In
our study, the negative 18F-FDG PET/CT group had small
tumor size and less common extrathyroid and lymphovas-
cular invasion. Therefore, this finding suggested that
J. W. Choi et al.
patients with PTCs with negative 18F-FDG PET/CT find-
ings preoperatively had good prognosis compared with
those with positive 18F-FDG PET/CT findings. In addition,
preoperative 18F-FDG PET/CT findings may predict the
prognosis of patients with PTC, and 18F-FDG PET/CT
positivity may be a useful prognostic factor.
In conclusion, our study showed that absence of peri-
thyroidal and lymphovascular invasion were independent
variables for false-negative findings on initial 18F-FDG
PET/CT in patients with PTCs. In addition, preoperative
negative 18F-FDG PET/CT findings may imply less
aggressive characteristics of primary PTC.
ACKNOWLEDGMENT This study was supported by a grant from
the National R&D Program for Cancer Control, Ministry for Health,
Welfare, and Family Affairs, Republic of Korea (0720560).
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