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BETHESDA  III  Atypies  de  significaDon  indéterminée  Lésion  folliculaire  de  significaDon  

indéterminée  

ETUDE ECHANTILLON % DE CARCINOMES SOUS-GROUPE SIGNE

ECHO CONCLUSION BIAIS

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BETHESDA  IV    

Néoplasme  folliculaire  Néoplasme  folliculaire    à  cellules  de  Hürthle  

ETUDE ECHANTILLON % DE CARCINOMES SOUS-GROUPE VALEUR

DIAGNOSTIQUE CONCLUSION COMMENTAIRES

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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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