Hindawi

Journal of yroid Research

Volume 2020, Article ID 8095378, 8 pages
https://doi.org/10.1155/2020/8095378

Research Article
The Bethesda System for Reporting Thyroid Cytopathology: A
Cytohistological Study

Bakiarathana Anand ,1 Anita Ramdas,1 Marie Moses Ambroise,1 and Nirmal P. Kumar2
1
Department of Pathology, Pondicherry Institute of Medical Sciences, Ganapathichettikulam, Kalapet, Puducherry 605014, India
2
Department of General Surgery, Pondicherry Institute of Medical Sciences, Ganapathichettikulam, Kalapet,
Puducherry 605014, India

Correspondence should be addressed to Bakiarathana Anand; bakiarathana24@gmail.com

Received 28 February 2020; Accepted 14 March 2020; Published 16 April 2020

Academic Editor: Brendan C. Stack Jr.

Copyright © 2020 Bakiarathana Anand et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Introduction. The Bethesda System for Reporting Thyroid Cytopathology (TBSRTC) is a significant step to standardize the
reporting of thyroid fine needle aspiration (FNA). It has high predictive value, reproducibility, and improved clinical significance.
Aim. The study was aimed to evaluate the diagnostic utility and reproducibility of “TBSRTC” at our institute. Methods and
Material. The study included 646 thyroid FNAs which were reviewed by three pathologists and classified according to TBSRTC.
Cytohistological correlation was done for 100 cases with surgical follow-up and the sensitivity, specificity, positive predictive
value, negative predictive value, diagnostic accuracy, and risk of malignancy (ROM) were calculated. The interobserver variation
among three pathologists was also assessed. Results. The distribution of cases in various TBSRTC categories is as follows:
I—nondiagnostic 13.8%, II—benign 75.9%, III—atypia of undetermined significance (AUS)/follicular lesion of undetermined
significance (FLUS) 1.2%, IV—follicular neoplasm (FN)/suspicious for follicular neoplasm (SFN) 3.7%, V—suspicious for
malignancy (SM) 2.6%, and VI—malignant 2.8%. The sensitivity, specificity, positive predictive value, negative predictive value,
and diagnostic accuracy are 72.4%, 94.3%, 84%, 89.2%, and 87.9%, respectively. The ROM of various TBSRTC categories were
II—8.5%; III—66.7%; IV—63.6%; and V and VI—100%. Cohen’s Weighted Kappa score was 0.99 which indicates almost perfect
agreement among the three pathologists. Conclusions. Our study substantiates greater reproducibility among pathologists using
TBSRTC to arrive at a precise diagnosis with an added advantage of predicting the risk of malignancy which enables the clinician
to plan for follow-up or surgery and also the extent of surgery.

1. Introduction organized the NCI Thyroid Fine Needle Aspiration State of

the Science Conference which proposed a 6-tier system and
Thyroid nodules are a common clinical problem. It is im- named it The Bethesda System for Reporting Thyroid
portant to differentiate benign from malignant nodules. Fine Cytopathology (TBSRTC). The categories and their risk of
needle aspiration (FNA) is utilized as a preoperative diag- malignancy for I—nondiagnostic, II—benign, III—atypia of
nostic technique which is safe, simple, and cost effective for undetermined significance (AUS)/follicular lesion of un-
triaging patients with thyroid nodules [1]. determined significance (FLUS), IV—follicular neoplasm
Proper communication among pathologists, clinicians, (FN)/suspicious for follicular neoplasm (SFN),
radiologists, and surgeons along with cytohistological cor- V—suspicious for malignancy (SM), and VI—malignant
relation is essential for reporting of thyroid FNA. Hence, were 1–4%, 0–3%, 5–15%, 15–30%, 60–75%, and 97–99%,
consistent diagnostic terminology is vital. respectively [2].
To achieve standardization of diagnostic terminology, The study aimed to evaluate the diagnostic utility and
morphologic criteria, and risk of malignancy for reporting of reproducibility of “The Bethesda System for Reporting
thyroid FNA, in 2007, the National Cancer Institute (NCI) Thyroid Cytopathology” at our institute.
2 Journal of Thyroid Research

2. Materials and Methods histopathology, 71 cases were confirmed to be benign of

which the most common was nodular goitre. Out of 100
All thyroid FNA smears and thyroidectomy specimens re- cases, 29 were malignant. Papillary carcinoma (17%) was the
ceived from January 2013 to June 2018 in the Department of most common malignancy followed by follicular carcinoma
Pathology, at our institute, were included in the study after (6%) (Table 2).
obtaining approval from the Institute Ethics Committee. The Risk of malignancy was assessed for 100 cases with
FNA smears were reviewed and categorized according to the surgical follow-up. Out of 100 cases, one was excluded since
Bethesda system. Cytohistological correlation was done for it was reported as nondiagnostic on cytology. To calculate
cases with surgical follow-up. the risk of neoplasm the surgical resections were divided into
Statistical analysis was performed using R software three groups: benign nonneoplastic lesions, benign neo-
version 3.5.1 (R Core Team) and Microsoft Office Excel 2007. plasms, and malignant lesions (Table 2).
Mean, median, and Standard Deviation (SD) were calculated
for continuous variables like age. Categorical variables were
expressed as frequencies and percentages. ANOVA test was 3.3. Determination of Diagnostic Values. The total of 99 cases
used to calculate the p value. A p value <0.05 was considered was divided into two groups. One group comprised of
statistically significant. Bethesda categories II and III for which surgery is not
The diagnostic values (sensitivity, specificity, positive recommended due to low malignancy risk and the other
predictive value, negative predictive value, and accuracy) group consisted of Bethesda categories IV, V, and VI for
and risk of malignancy for FNAs using the Bethesda system which surgery is recommended due to high malignancy risk.
were calculated for cases with surgical follow-up. FNA The sensitivity, specificity, positive predictive value, negative
smears interpreted as nondiagnostic were excluded. True predictive value, and diagnostic accuracy hence obtained are
negative cases were defined as nodules with benign FNA 72.4%, 94.3%, 84%, 89.2%, and 87.9%, respectively (Table 3).
cytology and surgical pathology. Follicular neoplasm/sus-
picious for follicular neoplasm, suspicious for malignancy, 3.4. Interobserver Agreement. Cross tabulation and Cohen’s
and malignant cases confirmed to be malignant upon final Weighted Kappa (κ) were applied to evaluate the concor-
histology were considered true positive. Nodules with cy- dance among the three observers. Cohen’s Weighted Kappa
tological results of FN/SFN or suspicious for malignancy or score was 0.99 which indicates almost perfect agreement
malignant diagnosed as benign on surgical excision were among the three pathologists.
interpreted as false positive. False negative samples included
cases with benign cytology that were found to be malignant 4. Discussion
upon histopathology.
Cross tabulation and Cohen’s Weighted Kappa (κ) were The goal of thyroid FNA is to successfully differentiate
applied to evaluate the concordance among the three ob- benign from malignant lesions and to triage patients re-
servers. The Kappa coefficient was interpreted as follows: quiring surgery. The six-tired Bethesda system provides
0–0.2 indicates poor agreement, 0.3–0.4 indicates fair standardized nomenclature for reporting thyroid FNA
agreement, 0.5–0.6 indicates moderate agreement, 0.7–0.8 smears which enables better communication and under-
indicates strong agreement, and >0.8 indicates almost standing between clinicians and pathologists. The advantage
perfect agreement. of this systematic approach is that each of the six Bethesda
categories has implied risk of malignancy which helps the
3. Results clinicians to plan appropriate therapy necessary for the
patient [3].
The study included 646 patients with complaints of thyroid Nondiagnostic (ND) thyroid FNA result remains a
swelling evaluated by FNA. The age group of the patients major constraint in arriving at a definitive diagnosis and is
ranged from 7 to 85 years with a mean of 41.78 years. The the most common cause of false negative reports [4]. It is
male: female ratio was 1 : 6.3. difficult to assess the risk of malignancy for the ND category
because only a small subset of ND nodules undergoes re-
3.1. Distribution of Cases according to the Bethesda System. section. Hence there is disparity in the malignancy rate
Out of 646 cases, 75.9% were benign of which 34.7% was among various studies which ranges from 0% to 63.2% [5, 6].
nodular goitre. Scant cellularity contributed with 7.8% of the Gunes et al. stated that the clinical expertise of the person
nondiagnostic category. The distributions of AUS/FLUS performing the FNA, ultrasound guidance, and rapid on-site
(III) and FN/SFN (IV) were 1.2% and 3.7%, respectively. evaluation for specimen adequacy were not uniform be-
Category-V constituted 2.4% cases suspicious for papillary tween studies which contributes to the wide range of ma-
carcinoma. Papillary carcinoma (2%) was the most common lignancy rate. All these determinants make the comparison
malignancy in category-VI (Table 1). between studies cumbersome and should be taken into
consideration while labelling a specimen as nondiagnostic
and assessing the risk of malignancy [4]. Some of the studies
3.2. Cytohistological Correlation with Assessment of Risk of stated that the operator experience and the number of passes
Malignancy and Risk of Neoplasm. Cytohistological corre- made during FNA correlate with the nondiagnostic result
lation was done for 100 patients with surgical follow-up. On [7, 8].
Journal of Thyroid Research 3

Table 1: Distribution of cases according to the Bethesda system.

Bethesda category No. of cases Percentage
Bethesda category FNA diagnosis
percentage (%) (total � 646) (%)
Cyst fluid 6 0.9
I—nondiagnostic (89) 13.8 Scant cellularity 50 7.8
Obscuring blood 33 5.1
Nodular goitre 224 34.7
Adenomatoid nodule 37 5.7
Colloid nodule 70 10.8
II—benign (490) 75.9
Grave’s disease 3 0.5
Lymphocytic (Hashimoto)
156 24.2
thyroiditis
III—AUS/FLUS (8) 1.2 AUS/FLUS 8 1.2
IV—FN/SFN (24) 3.7 FN/SFN 24 3.7
Suspicious for papillary
16 2.4
V—suspicious for malignancy carcinoma
2.6
(17) Suspicious for medullary
1 0.2
carcinoma
Papillary carcinoma 13 2.0
Medullary carcinoma 3 0.4
VI—malignant (18) 2.8
Poorly differentiated carcinoma 1 0.2
Undifferentiated carcinoma 1 0.2

In our study, the nondiagnostic yield was 13.8% which Mondal et al. reported a lower percentage (1%) of AUS/
was high when compared to TBSRTC consensus. Sampling FLUS cases which was a result of performing ultrasound
error and technical quality due to the above-mentioned guided FNA in small and heterogeneous nodules with
reasons and strict adherence to the adequacy criteria explain suspicious features on palpation and radiological evaluation,
the high rate of ND smears. so that the aspirate can be obtained from the exact site of
Mondal et al. and Nandedkar et al. found high incidence lesion which is a routine practice even at our institute [6].
of category II lesions since the patients directly visit a tertiary The actual risk of malignancy of category III is difficult to
care center for primary diagnosis without any referral which determine, since confirmatory diagnosis is only available in a
was also the case in our study [6, 9]. subset of patients selected for surgery who have suspicious
The incidence of benign lesions in our study was 75.9% clinical or USG features. The patients are also subjected to
when compared to studies done in USA ranging from 64% to selection bias which overestimates the prevalence of ma-
66% which can be attributed to the regional variation in the lignancy [15].
incidence of thyroid disorders and where majority of pa- The risk of malignancy of AUS/FLUS cases was 69% in a
tients come only on a referral basis and hence are not exactly study done by Park et al. which was higher when compared
representative of the general population [10, 11]. to our study and TBSRTC guidelines. This was because
The implied risk of malignancy for category II is 0% to patients with high index of clinical suspicion for malignancy
3% with the recommended management being clinical undergo surgery without a repeat FNA. Patients tend to be
follow-up of patients [2]. Although surgery is not recom- more concerned about false positive results than false
mended for category II lesions, the patients in our study were negative results, which might have pressurized cytopa-
operated mainly for cosmetic purpose and pressure thologists to underdiagnose cases to avoid making false
symptoms. positive diagnosis [16].
The indeterminate category, AUS/FLUS, has led to Our study was held in a teaching hospital, where FNAs
confusion due to inconsistent usage amongst pathologists of were performed by different persons with varied level of
various institutions. This category should be used as a last experience during their training period. This factor could
resort in reporting with the expectation of 7% or less cases to have resulted in hemodilution and artefactual changes
receive this diagnosis as proposed by TBSRTC. Layfield et al. during smear preparation which might have contributed to a
reported a variation of 2.5–28.6% among individual pathol- higher ROM in category III (Figure 1). Repeat FNAs of such
ogists and 3.3–14.9% among three academic institutions [12]. cases along with clinicoradiological correlation could have
There were less number of cases (1.2%) diagnosed under decreased the proportion of cases reported in this category as
the category AUS/FLUS in our study which was due to rigid well as the ROM.
adherence to the diagnostic criteria and the pathologists Based on cytology it is difficult to distinguish follicular
endeavor to avoid ambiguity and keep the use of AUS/FLUS carcinoma from follicular adenoma [2, 12] (Figure 2). Melo-
to a minimum which was in similarity to a study by Nan- Uribe et al. correlated the results of thyroid FNA reported
dedkar et al. which had 0.8% of cases in category III out of using the TBSRTC with histopathology, from three different
606 FNA’s [9]. Jo et al. and Yassa et al. have reported 3.4% hospitals in Columbia. There was significant variation in the
and 4% lesions as AUS/FLUS, respectively [13, 14]. malignancy risk of category IV which measured 56.3% in
 4

Table 2: Cytohistological correlation with assessment of risk of malignancy and risk of neoplasm.
Cases that Histopathology diagnosis
Risk of Risk of malignancy Risk of malignancy
No. of cases underwent
Bethesda category Benign Benign neoplasm including papillary excluding papillary
(total � 646) surgery Malignant lesion
nonneoplastic neoplastic (%) microcarcinoma (%) microcarcinoma (%)
(total � 100)
I—non diagnostic 89 (13.8%) 1 Colloid nodule (1) 0 0 0 0 0
Follicular
Nodular goitre (42)
carcinoma (1)
Adenomatoid Papillary carcinoma
hyperplasia (10) (2)
Follicular
II—benign 490 (75.9%) 71 Papillary 14.1 8.5 5.6
Colloid nodule (5) adenoma (4)
microcarcinoma (2)
Lymphocytic/
Hurthle cell
Hashimoto
carcinoma (1)
thyroiditis (4)
Follicular
Follicular carcinoma (1)
III—AUS/FLUS 8 (1.2%) 3 100 66.7 66.7
adenoma (1) Papillary carcinoma
(1)
Follicular Follicular
adenoma (1) carcinoma (4)
Papillary carcinoma
IV—FN/SFN 24 (3.7%) 11 Nodular goitre (2) 81.8 63.6 63.6
Hurthle cell (2)
adenoma (1) Medullary
carcinoma (1)
Papillary carcinoma
(5)
V—suspicious for Papillary
17 (2.6%) 7 100 100 85.7
malignancy microcarcinoma (1)
Medullary
carcinoma (1)
Papillary carcinoma
VI—malignant 18 (2.8%) 7 100 100 100
(7)
Journal of Thyroid Research
Journal of Thyroid Research 5

Table 3: Determination of diagnostic values. (Table 2). This was due to repeat FNA of cases with high
HPE HPE
index of clinical and ultrasound features suspicious for
Test Total malignancy.
malignant benign
The RON of category II was similar to the study done by
FNA Bethesda categories IV,
21 4 25 Wu et al. (Table 4) [20]. This was due to false negative
V, VI
FNA Bethesda categories II, reporting of 2 papillary microcarcinoma, 1 Hurthle cell
8 66 74 carcinoma, and 1 follicular carcinoma as benign. Two cases
III
Total 29 70 99 of conventional papillary carcinomas were misdiagnosed as
benign due to sampling error (Table 2). Follicular carcinoma
and Hurthle cell carcinoma are difficult to diagnose on FNA
and need to be confirmed by histopathology. Papillary
microcarcinoma is a lesion that measures 1 cm or less which
can be easily missed on FNA unless the aspirator hits the
target.
Our study was able to accurately predict the RON of
categories III, V, and VI when compared to the study done
by Wu et al. which could be attributed to the routine practice
of correlating cytology with clinical, biochemical, and ra-
diological features at our institute (Table 4) [20].
The FN/SFN category had RON of 81.8% which was high
compared to the study by Wu et al. This was due to clas-
sification of two cases of nodular goitre as category IV lesion
(Table 2). Another possible reason could be the variation in
sample size and less number of cases with surgical follow-up
in our study (Table 4) [20].
Mehra and Verma in their study found that the method
Figure 1: Atypia of undetermined significance (Bethesda category
of statistical analysis can alter the results of diagnostic values.
III). Smear shows clotting artefact with crowding of follicular cells
hindering the interpretation (MGG stain ×400).
If suspicious lesions are considered positive, the sensitivity
increases while the specificity decreases. If suspicious lesions
are excluded, then the sensitivity decreases and the false
oncology centers and 23.5% in nononcology centers which negative rates increase. In their study diagnostic values were
was attributed to the selection bias of the patients requiring calculated by either excluding FN/SFN or including it with
surgery [17]. either benign or malignant diagnosis to highlight the effect
The high ROM in categories III and IV in our study when on diagnostic values [21].
compared to other studies may be due to the following Shi et al. suggested that eliminating the diagnosis of
reasons. Firstly, it is due to the heterogeneity of the inde- category III substantially decreases the sensitivity of thyroid
terminate categories III and IV which are subject to variation FNAs (the sensitivity for detecting PTC dropped from 100%
in interpretation across institutions [3]. Secondly, it is be- to 27%) and increases both false positive and false negative
cause of variations in number of patients with surgical rates. The authors concluded that AUS/FLUS category
follow-up and also the selection bias of patients requiring should not be eliminated but recommended using it min-
surgery. imally [22].
Our study had 2.4% cases suspicious for papillary thy- The findings from our study indicate that the calculation
roid carcinoma (PTC) which was similar to the lower range of sensitivity, specificity, positive predictive value, negative
of rate of suspicious for PTC in the following study [15]. The predictive value, and diagnostic accuracy of thyroid FNAs
ROM of category V in a study by Williams et al. was less according to the Bethesda system are less reliable because of
when compared to our study which may be due to variation the arbitrary nature of cases classified under categories III
in cohort characteristics and underdiagnoses of lesions (AUS/FLUS) and IV (FN/SFN) (Table 3).
leading to hemithyroidectomy rather than total thyroidec- The main purpose of TBSRTC was to eliminate the
tomy [18]. ambiguity and to follow uniformity in the reporting of
The ROM in a study by Partyka et al. was in good thyroid FNAs thereby enabling ease of communication
correlation with our study in categories V and VI which was among pathologists and clinician and to plan appropriate
100% each after inclusion of papillary microcarcinoma [19] treatment for the patients [2]. Table 5 shows comparison of
(Figure 3). Our study was able to accurately predict the ROM interobserver reproducibility of our study with that of other
for suspicious for malignancy and malignant nodules due to studies [23–25].
the practice of correlating cytologic features with clinical, Our study differed from a study done by Padmanabhan
biochemical, and USG findings while reporting (Table 2). et al. which assessed the interobserver reproducibility in
The risk of neoplasm (RON) gives an overall estimate of reporting AUS/FLUS category among seven cytopatholo-
predicting both benign and malignant lesions. Our study gists which revealed fair agreement (Fleiss kappa score 0.23)
had nil risk of neoplasm in the nondiagnostic category and recommended review of AUS/FLUS cases for more
6 Journal of Thyroid Research

(a) (b)

(c)

Figure 2: Follicular neoplasm/suspicious for follicular neoplasm (Bethesda category IV). (a) Highly cellular smear with cells arranged
predominantly in microfollicular pattern (MGG ×100). Histopathology of the same showed follicular carcinoma with capsular invasion (b)
and vascular invasion (c) (H&E ×100).

(a) (b)
Figure 3: Continued.
Journal of Thyroid Research 7

(c) (d)

Figure 3: Suspicious for papillary carcinoma (Bethesda category V). (a) One of the follicular cells show nuclear groove (arrow) (H&E ×400).
(b) Intranuclear cytoplasmic inclusion (arrow) seen in occasional follicular cell (H&E ×400). (c) Smear shows focal papillaroid structure
(H&E ×400). (d) Histopathology of the same showed papillary microcarcinoma (H&E ×100).

Table 4: Comparison of risk of neoplasm of our study with another study by Wu et al. [20].
Bethesda category Risk of neoplasm of our study (%) (n � 100/646) Risk of neoplasm in a study by Wu et al. (%) (n � 221/1382)
I—nondiagnostic 0 24
II—benign 14.1 14
III—AUS/FLUS 100 44
IV—FN/SFN 81.8 67
V—SFM 100 77
VI—malignant 100 100

Table 5: Comparison of interobserver reproducibility of among various studies.

Study No. of observers Interobserver agreement
Awasthi et al. [23] 2 Good (Cohen’s kappa score 0.613)
Padmanabhan et al. [25] 7 Fair (Fleiss kappa score 0.23)
Pathak et al. [24] 3 Strong (Fleiss kappa score 0.6561)
Our study 3 Almost perfect (Cohen’s kappa score 0.99)

definite categorization [25]. We observed a trend that the Additional Points

less the number of observers (2-3), the more the chance of
interobserver agreement (Table 5). The yield of nondiagnostic aspirate was high due to the
varied experience level of the persons who performed the
thyroid FNA. Repeat USG guided FNA would have reduced
5. Conclusion the number of nondiagnostic aspirates but it was feasible
only for patients with high index of clinical and radiological
Thyroid FNA smears reported using the Bethesda system
features suspicious of malignancy.
helped in achieving more precise cytological diagnosis. Our
study substantiates greater reproducibility among patholo-
gists using TBSRTC for reporting thyroid FNA. The Conflicts of Interest
Bethesda system has an added advantage of predicting the
risk of malignancy which enables the clinician to plan for The authors declare that they have no conflicts of interest.
follow-up or surgery and also the extent of surgery.
Acknowledgments
Data Availability The authors would like to thank the Department of Pa-
The raw data used to support the findings of this study have thology, Pondicherry Institute of Medical Sciences for their
not been made available because of patient’s confidentiality guidance and support, and Dr. Anand Mariaselvam, Medical
and privacy rules. Officer, Indira Gandhi Government General Hospital and
8 Journal of Thyroid Research

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[16] J. H. Park, S. O. Yoon, E. J. Son, H. M. Kim, J. H. Nahm, and
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