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no significant difference in the percentages of malignant nodules
with microcalcifications or increased intranodular vascularity
when compared to benign nodules. The malignancy rate based
on TIRADS categories is shown in Table 3. There were no nod-
ules scored as TIRADS 3 in our study. The risk of malignancy
increased with advancing TIRADS score: TIRADS 4A (14!3%),
TIRADS 4B (23!1%), TIRADS 4C (87!5%) and TIRADS 5
(100%) (Table 3). The malignancy rate of each TIRADS cate-
gory (calculated based on the recently proposed prediction
model)15 similarly increased with advancing TIRADS score: TIR-
ADS 4A (6!2%), TIRADS 4B (32!5%), TIRADS 4C (79!9%) and
TIRADS 5 (90%). A comparison of malignancy risk based on
the risk prediction model and histological outcomes in each
TIRADS category is shown in Fig. 1.
Discussion
The diagnosis of follicular neoplasm (Thy3F) remains a diagnos-
tic dilemma. The distinction of follicular adenoma from follicu-
lar carcinoma requires the presence of capsular or vascular
invasions but such characteristics cannot be assessed on cytologi-
cal evaluation. In our study, the majority of the nodules with
Thy3F cytology were benign, which were mostly follicular ade-
nomas on histology. Although there were a significant propor-
tion of papillary thyroid cancers among the malignant nodules,
four of these were follicular variants of papillary thyroid cancers.
It is well known that the cytological diagnosis of this entity is
often challenging to make, and it can be misdiagnosed as follicu-
lar neoplasms on FNAC.16
The current British Thyroid Association guidelines recom-
mends repeat FNA for Thy3A cytology results, but a diagnostic
hemithyroidectomy remains the next step in the evaluation of
Thy3F cytology outcomes.3 The overall malignancy rate of nod-
ules with Thy3F cytology result was 24!3% in our study, which
is similar to the malignancy rate for this cytological category
based on the current guidelines.1 Hence, the fact that majority
of these cases have benign disease on postoperative histology
justifies the effort to better select candidates for surgery.
Ultrasound is an important diagnostic tool in predicting thy-
roid malignancy and selecting thyroid nodules that should be
evaluated by FNA. Known suspicious US features include
hypo-echogenicity, microlobulated or irregular margins, micro-
calcifications and a taller-than-wide shape. Although no single
US feature can reliably predict the risk of malignancy, a
combination of these features is known to provide better
Table 1. Histological diagnosis in the 144 cases
Histological diagnosis N (%)
Benign 109 (75!7%)
Follicular adenoma 57Hurthle cell adenoma 3
Multinodular goitre/Nodular hyperplasia 21Hyperplastic nodule 27
Intrathyroid parathyroid adenoma 1Malignant 35 (24!3%)
Papillary thyroid cancer 15Follicular thyroid cancer 16
Both papillary and follicular thyroid cancer 3
Medullary thyroid cancer 1
Table 2. Comparison of patient demographics and sonographiccharacteristics between thyroid nodules with benign and malignant
histology
Benign (n = 109) Malignant (n = 35) P-value
Demographic characteristicsMean age (years) 44!1 " 14!9 49!6 " 15!7 0!061Male 23 (67!6%) 11 (32!4%)Female 86 (78!2%) 24 (21!8%) 0!153
Sonographic characteristicsNodule size (cm) 2!8 " 1!5 3!2 " 1!5 0!222Irregular margins 0 7 (20!0%) 0!000*Hypo-echogenicity 56 (51!4%) 26 (74!3%) 0!013*Taller-than-widemorphology
1 (0!9%) 6 (17!1%) 0!001*
Presence of
microcalcifications
5 (4!6%) 3 (8!6%) 0!302
Intranodular
vascularity
55 (50!5%) 17 (48!6%) 0!500
*Denotes statistical significant results.
Table 3. Malignancy rate based on TIRADS category in the 144 caseswith diagnosis of follicular neoplasm on cytology
TIRADScategory
No of cases(n) Benign (n, %)
Malignant(n, %)
Malignantrate (%)
4A 56 48 (44!0%) 8 (22!9%) 14!34B 78 60 (55%) 18 (51!4%) 23!14C 8 1 (0!9%) 7 (20!0%) 87!55 2 0 (0%) 2 (5!7%) 100
Total 144 109 35 24!3
14· 323· 1
87· 5
100
6· 2
32· 5
79· 990
0
20
40
60
80
100
120
4A 4B 4C 5M
alig
nanc
y ra
te (%
)
TIRADS category
Malignant rate based on histology
Malignancy rate based onrisk predic!on model
Fig. 1 Graph comparing the malignancy rate of various TIRADScategory calculated by the histology results of our study and malignancy
rate calculated using the risk prediction model proposed by Kwaket al.15
© 2014 John Wiley & Sons LtdClinical Endocrinology (2014), 0, 1–6
Predictors of malignancy in thyroid follicular neoplasms 3
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the needle were sequentially fired. Tissue cores were placedin 10% buffered formalin immediately after the procedureand then conventionally processed (10). The adequacy of theprocedure was assessed using real-time US imaging, and theadequacy of the specimens was assessed visually. To be ad-equate, all negative smears had to contain at least 6 groups ofepithelial cells with 10 cells per group for FNA and anyidentifiable thyroid tissue for CNB (9,10).
Additional FNA or CNB procedures were performed whena lesion was considered inaccurately targeted in the case ofsmall nodules or when an insufficient specimen was sus-pected by visual inspection (10). After the biopsy, each pa-tient was observed while using firm, local compression of thebiopsy site for 10–20 minutes. When a patient complained ofpain or swelling of their neck, a repeat US examination wasperformed to evaluate these complications (10).
Cytology and histology analysis
FNA cytology and CNB histology specimens were re-viewed by experienced pathologists. FNA cytology diagnoseswere categorized into six categories according to the BethesdaSystem for Reporting Thyroid Cytopathology (15) (i.e., non-diagnostic, benign, AUS/FLUS, FN/SFN, suspicious formalignancy, and malignancy). As our hospital has used theBethesda System for FNA cytology diagnoses since 2012, wehave replaced all cytology readings made prior to 2012. Asthe diagnostic criteria of CNB have not yet been standardizedfor thyroid nodules, CNB histology diagnoses were categorizedinto the same six Bethesda System categories in accordancewith the CNB histopathology results (9,10). The FN readingsobtained from FNA and CNB procedures included nodules withhistology features favoring follicular neoplasm (16).
Statistical analysis
Statistical analysis was performed using statistical soft-ware (SPSS, version 11.0; SPSS, Chicago, IL). The v2 testand the unpaired Student’s t test were used to compare de-mographic data between the FNA and CNB group (i.e., age,sex, mean nodule size, mean number of biopsies). The v2 testor the Fisher’s exact test was used to compare the false-positive rate (i.e., positive predictive value and unnecessarysurgery rate in the FNA and CNB groups) in accordance withthe final diagnosis. The false-positive rate was defined as thefinal diagnosis of non-neoplasms, including nodular hyper-plasia or thyroiditis. The true-positive rate was defined as thefinal diagnosis of a neoplasm (other than nodular hyperplasiaor thyroiditis). The unnecessary surgery rate was calculatedbased on the false-positive rate, after excluding patients forwhom surgery was inevitable, such as cases with a coexisting,known papillary thyroid carcinoma or a cosmetic problemcaused by the large size of a thyroid nodule. The v2 test orFisher’s exact test was also used to compare the malignancyrates between the FNA and CNB groups. A p value < 0.05was considered statistically significant.
Results
Demographic characteristics
The demographic characteristics are summarized in Ta-ble 1. In the FNA group, there were 24 men (mean age, 52.8
years; age range, 31–72 years) and 83 women (mean age,45.9 years; age range, 19–70 years). In the CNB group, therewere 29 men (mean age, 51.2 years; age range, 13–83 years)and 78 women (mean age, 44.5 years; age range, 16–74years). There was no significant difference in age or sex be-tween the two groups. The mean nodule size was 2.2 cm(range, 0.4–19.6 cm) in the FNA group and 2.9 cm (range,0.6–13 cm) in the CNB group, which showed a significantdifference ( p < 0.001). There were 9 nodules of less than 1 cmin the FNA group and 5 nodules in CNB group. The meannumber of biopsies was significantly greater in the FNAgroup than in the CNB group ( p = 0.016). In all patients, CNBprocedures were tolerable and were fully completed withoutimmediate complications. There was no evidence of majorcomplications resulting in hospitalization, such as hematoma,infection, or pain after CNB.
Final diagnosis of FNA and CNB with FN reading
Among the patients with FN readings, 52.7% (107/231) inthe FNA group and 57.5% (107/180) in the CNB group un-derwent surgery. The number and proportion of the final di-agnosis after surgery in the FNA and CNB groups are listed inTable 2. The false-positive, unnecessary surgery, and ma-lignancy rates in each group are shown in Table 3. CNBshowed a significantly lower false-positive rate than FNA
Table 1. Demographic Characteristicsof the Fine-Needle Aspiration
and Core-Needle Biopsy Groups
Characteristics FNA (n = 107) CNB (n = 107) p Value
Mean age(range)
47.4 (19–72) 46.3 (13–83) 0.532
Sex (M:F) 24:83 29:78 0.428Mean nodule
size of (cm)2.2 (0.4–19.6) 2.9 (0.6–13) < 0.001
Mean numberof biopsies
1.4 (1–5) 1.2 (1–3) 0.016
A p value of < 0.05 was considered statistically significant.FNA, fine-needle aspiration; CNB, core-needle biopsy.
Table 2. Comparison of the Final Diagnosesin the Fine-Needle Aspiration
and Core-Needle Biopsy Groups
Final diagnosis FNA (n, %) CNB (n, %) p Value
Neoplasm 74 (69.2) 102 (95.3) < 0.001Follicular adenoma 35 (32.7) 34 (31.8) 0.884Hurthle cell adenoma 9 (8.4) 6 (5.6) 0.422Follicular carcinoma 12 (11.2) 37 (34.6) < 0.001Hurthle cell
carcinoma3 (2.8) 4 (3.7) > 0.99
FVPTC 9 (8.4) 16 (15) 0.579PTC 6 (5.6) 5 (4.7) 0.757
Non-neoplasm 33 (30.8) 5 (4.7) < 0.001
A p value of < 0.05 was considered statistically significant.FNA, fine-needle aspiration; CNB, core-needle biopsy; FVPTC,
follicular variant papillary thyroid carcinoma; PTC, papillarythyroid carcinoma.
1614 YOON ET AL.
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