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253
CANCER
CYTOPATHOLOGY
Fine-Needle Aspiration of Thyroid Nodules
Correlation between Cytology and Histology and Evaluation of Discrepant Cases
Mary K. Sidawy, M.D.1
David M. Del Vecchio, M.D.3
Stanley M. Knoll, M.D.2
BACKGROUND. The purpose of this study was to evaluate the results of thyroid
fine-needle aspiration (FNA) and to determine the reasons for the discrepancies
between the cytologic and histologic diagnoses.
METHODS. The authors evaluated the cytologic and histologic results of 133 FNAs
1
Department of Pathology, The George Washington University Medical Center, Washington,
DC.
2
Department of Surgery, The George Washington University Medical Center, Washington, DC.
3
Department of Pathology, Naval Medical Center, Portsmouth, Virginia.
obtained from 92 patients who underwent subsequent thyroidectomies.
RESULTS. The initial cytologic results were indeterminate in 39 of 133 cases (29%)
because a neoplasm could not be ruled out. These cases corresponded histologically to 9 adenomatoid nodules (ANs), 14 follicular adenomas (FAs), and 16 malignant thyroid neoplasms. The reported FNA diagnoses of the remaining 94 cases
(71%) were 48 ANs, 19 follicular neoplasms (FNs), 21 papillary carcinomas (PCs),
and 6 cases of Hashimoto’s thyroiditis (HT). Correlation of cytology and histology
showed that 69 of 94 FNA results (73%) correlated with the histologic diagnoses,
whereas 25 (27%) were discrepant. The discrepancies resulted from cytodiagnostic
errors in 13 cases (52%), suboptimal smears in 11 (44%), and an FNA sampling
error in 1 (4%). The false-negative rate of FNA was 19% and the false-positive rate
was 6%.
CONCLUSIONS. Diagnostic pitfalls and indeterminate FNA diagnoses were predominantly due to overlapping cytologic criteria between ANs, FNs, and follicular variants of PCs. Rendering a definite diagnosis on suboptimal FNA samples is also a
significant source of pitfalls. Cancer (Cancer Cytopathol) 1997;81:253–9.
q 1997 American Cancer Society.
KEYWORDS: fine-needle aspiration, thyroid, accuracy, diagnostic pitfalls, adequacy.
C
Address for reprints: Mary K. Sidawy, M.D., Department of Pathology, The George Washington
University Medical Center, Ross Hall #419, 2300
Eye Street, N.W., Washington, DC 20037.
The views expressed in this article are those of
the authors and do not reflect the official policy
or position of the Navy, the Department of Defense, or the United States Government.
Received May 15, 1997; accepted May 19,
1997.
linically detectable thyroid nodules occur in approximately 4 – 10%
of the population; however, only 5 – 30% of the nodules are malignant.1,2 Fine-needle aspiration (FNA) is a well-established diagnostic
procedure that is often used as one of the initial screening tests for
patients with thyroid nodules. It is recognized that aside from surgical
excision, FNA offers the best predictive value of any test currently
available.1,3 The main goal of thyroid FNA is to identify nodules that
require surgery. Its impact on the management of thyroid nodules
has resulted in an overall decrease in the number of thyroidectomies
performed on cold nodules, with a concomitant increase in the yield
of malignancy for resected thyroid nodules.4 – 7 Nevertheless, FNA has
some limitations, and both false-positive and false-negative results
occur. The current study was undertaken to evaluate the correlation
between cytology and histology in thyroid FNA in our laboratory and
to determine the sources of diagnostic errors.
MATERIALS AND METHODS
We reviewed the results of 139 FNAs obtained from 96 patients who
underwent subsequent thyroidectomies at the George Washington
q 1997 American Cancer Society
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254
CANCER (CANCER CYTOPATHOLOGY) August 25, 1997 / Volume 81 / Number 4
FIGURE 1. This figure shows the correlation between the cytology and histology of the 133 fine-needle aspirations (FNAs) included
in this study and the results of retrospective review of the discrepant cases. AN: adenomatoid nodule; HT: Hashimoto’s thyroiditis;
FA: follicular adenoma; FC: follicular carcinoma; PC: papillary carcinoma; FV: follicular variant of PC; MC: medullary carcinoma.
University Medical Center. Because a significant number of patients whose thyroid FNAs are evaluated in
our laboratory (approximately 550 per year) are referred elsewhere for surgery, the study population was
derived from the files of one of the authors (S.M.K.),
a surgeon, who refers his FNAs to our Cytopathology
Service and operates in our hospital. Therefore, both
cytologic and histologic materials were available for
review. The study period extended over 52 months
(May 1988 to September 1992). The ages of the patients
ranged from 22 to 81 years. The FNAs were distributed
among 78 women (115 FNAs) and 18 men (24 FNAs).
At our institution, the majority of thyroid FNAs are
classified as adenomatoid nodules (ANs) with or without cystic change, Hashimoto’s thyroiditis (HT), papillary carcinomas (PCs), follicular neoplasms (FNs), and
medullary carcinomas (MCs). Less common entities
include anaplastic carcinomas, lymphomas, and metastases. FNs include both follicular adenomas (FAs)
and follicular carcinomas (FCs); we do not attempt to
distinguish between these two entities cytologically.
Such distinction requires histologic evidence of capsular or vascular invasion.
The original FNA results were classified as ‘‘diagnostic’’ when the smears were classified into one of the
above diagnostic categories and as ‘‘indeterminate’’
when a definite cytologic diagnosis was not made (i.e.,
when a neoplasm could not be ruled out). The definition of ‘‘indeterminate’’ is based on the fact that what
determines the need for surgery is a diagnosis of a
neoplastic versus a nonneoplastic lesion (an FNA result that cannot be used to make that distinction is
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considered indeterminate). The FNAs included in the
study contained a minimum of 10 clusters of wellvisualized follicular cells with at least 20 cells in each
cluster on 2 or more slides. Six indeterminate FNAs
from four patients were reported as ‘‘cystic lesions not
further classified due to paucity or absence of epithelial cells.’’ The subsequent thyroidectomies revealed
four ANs and two FAs. These cases were excluded from
the study.
The cytologic diagnoses were compared with the histologic diagnoses. FNAs with diagnostic results were categorized as either ‘‘correlate’’ or ‘‘discrepant.’’ The cytologic smears and the histologic sections of the discrepant
cases were retrospectively reviewed to determine whether
the discrepant diagnosis was attributed to histologic misinterpretation, cytodiagnostic error (misinterpretation of
established criteria or overlapping criteria among the entities), sampling error of the lesion by FNA, or smears of
suboptimal quality (limited by poor cellular preservation,
partially obscured by blood, diluted, or having borderline
cellularity).
False-negative and false-positive results were evaluated using the definitions proposed in the recently
published guidelines of the Papanicolaou Society of
Cytopathology.8 These definitions are based on patient
management outcome. A false-negative diagnosis is
defined as a diagnosis of a nonneoplastic lesion, which
does not usually require surgical intervention, rendered on a malignant lesion. A false-positive cytologic
diagnosis is defined as a diagnosis of a neoplasm,
which requires surgical excision, rendered on a nonneoplastic lesion.8
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Cytology and Histology of Thyroid FNA/Sidawy et al.
255
TABLE 1
Correlation between Cytology and Histology in Indeterminate FNA Cases
Histologic dx
FNA dx
AN
FA
FC
PC
FV
MC
Total
AN vs. FN
SFN
SPC
STN
7
0
0
2
6
5
2
1
4
0
0
0
0
3
4
0
2
2
0
0
0
0
0
1
19
10
6
4
Total
9
14
4
7
4
1
39
FNA: fine-needle aspiration; dx: diagnosis; AN: adenomatoid nodule; FN: follicular neoplasm; SFN: suspicious for follicular neoplasm; SPC: suspicious for papillary carcinoma; STN: suspicious for thyroid neoplasm;
FA: follicular adenoma; FC: follicular carcinoma; PC: papillary carcinoma; FV: follicular variant of papillary carcinoma; MC: medullary carcinoma.
TABLE 2
Comparison of the Cytologic and Histologic Diagnoses of the 25 Discrepant Cases
Histologic dx
FNA dx
AN
FA
FC
PC
FV
HT
Total
AN
FN
PC
HT
0
2
0
0
11
0
0
0
3
0
0
0
0
1
0
2
4
1
0
0
0
0
1
0
18
4
1
2
Total
2
11
3
3
5
1
25
AN: adenomatoid nodule; FN: follicular neoplasm; PC: papillary carcinoma; HT: Hashimoto’s thyroiditis; FA: follicular adenoma; FC: follicular carcinoma; FV: follicular variant of papillary carcinoma.
RESULTS
The study included 133 FNAs from 92 patients. It is
important to emphasize that the proportion of various
lesions in this series of FNAs with subsequent thyroidectomies does not reflect the overall proportion of diagnoses rendered by the laboratory. The FNA results,
the correlation between cytology and histology, and
the retrospective review of the discrepant cases are
presented in algorithmic form in Figure 1. The original
cytologic results were indeterminate in 39 of 133 cases
(29%). These indeterminate FNA cases corresponded
histologically to 9 ANs and to 14 benign and 16 malignant thyroid neoplasms (Table 1). FNAs yielded a diagnostic result in 94 of 133 cases (71%): 48 ANs, 19 FNs,
21 PCs, and 6 cases of HT. Of these 94 diagnostic FNAs,
69 (73%), consisting of 30 ANs, 15 FNs (12 FAs and 3
FCs histologically), 20 PCs, and 4 cases of HT, correlated with the histologic diagnoses, and the remaining
25 FNAs (27%) were discrepant (18 ANs, 4 FNs, 1 PC,
and 2 cases of HT). Table 2 summarizes the comparisons between the cytologic and histologic diagnoses
of the discrepant cases. On review of the histologic
sections of the 25 discrepant cases, the rendered histo-
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logic diagnoses remained unchanged. Twenty histologically proven thyroid neoplasms (11 FAs, 3 FCs, 2
PCs, and 4 FVs) were diagnosed cytologically as ANs
or HT. Nine of these 20 cases were malignant and
therefore considered false-negative. False-positive results occurred in three FNAs, which were interpreted
as FNs in two cases and PC in one case, and revealed
AN and HT histologically. The remaining two discrepancies consisted of misclassification of a histologically
proven PC and an FV as FN cytologically. Therefore,
the false-negative rate of FNA in our series was 19%,
and the false-positive rate was 6%.
Retrospective review of the cytologic material of
the discrepant cases showed that the discrepancies
resulted from cytodiagnostic errors in 13 cases (52%),
suboptimal quality of cytologic material in 11 (44%),
and FNA sampling error in 1 (4%). The latter case was
diagnosed as HT by FNA and revealed a 0.8 cm PC in
the midst of chronic lymphocytic thyroiditis histologically. These results are summarized in Table 3. The
cytodiagnostic errors were attributed to misinterpretation in 6 of 13 cases (3 histologically proven FAs, 2
PCs, and 1 case of HT) and to overlapping cytologic
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CANCER (CANCER CYTOPATHOLOGY) August 25, 1997 / Volume 81 / Number 4
TABLE 3
Source of Error in the 25 Discrepant Cases
Histologic dx
Error
AN
FA
FC
PC
FV
HT
Total
Diagnostic
Suboptimala
Sampling
2
0
0
3
8
0
1
2
0
2
0
1
4
1
0
1
0
0
13
11
1
Total
2
11
3
3
5
1
25
AN: adenomatoid nodule; FA: follicular adenoma; FC: follicular carcinoma; PC: papillary carcinoma; FV: follicular variant of papillary carcinoma; HT: Hashimoto’s thyroiditis.
a
Attributed to suboptimal quality of smear.
FIGURE 2.
This figure shows cytodiagnostic errors due to overlapping
cytologic features among adenomatoid nodules, follicular neoplasms, and
follicular variant of papillary carcinomas. (A) Fine-needle aspiration (FNA)
is interpreted as an adenomatoid nodule based on the presence of flat sheets
of follicular cells with minimal nuclear overlap and no evidence of acinar or
rosette formation. Thyroidectomy revealed a follicular adenoma (Diff-Quik,
original magnification 1400). (B) FNA was interpreted as a follicular neoplasm based on the presence of a repetitive acinar pattern and microfollicles.
Thyroidectomy revealed a follicular variant of papillary carcinoma (Diff-Quik,
original magnification 11000). (C) FNA was interpreted as a follicular neoplasm based on the presence of nuclear enlargement, overlap, and microfollicle formations. Thyroidectomy revealed an adenomatoid nodule (Diff-Quik,
original magnification 11000).
criteria in 7 cases (2 histologically proven ANs, 1 FC,
and 4 FVs). Examples of cytodiagnostic errors are illustrated in Figures 2 and 3.
DISCUSSION
The sensitivity of thyroid FNA ranges from 65% to 99%
and its specificity from 72% to 100%.9 – 13 The reported
false-negative rate ranges from 1% to 11%.4,7,10,13 However, it is difficult to know the true frequency of falsenegative results because only a small percentage (ap-
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proximately 10%) of patients with benign cytologic
findings undergo surgery.13 Most authorities agree that
the true false-negative rate is below 5% if all patients
with thyroid FNA also have a histologic examination.13
Because FNA is considered a screening procedure,
particular attention should be given to minimizing
false-negative diagnoses, even at the expense of accepting false-positive diagnoses.8
In the current study, the FNA results were diagnostic in 71% and indeterminate in 29% of the cases.
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Cytology and Histology of Thyroid FNA/Sidawy et al.
FIGURE 3. A cytodiagnostic error due to an interpretative error is represented. A fine-needle aspiration (FNA) was reported as Hashimoto’s thyroiditis. Thyroidectomy showed a 1.5 cm Hürthle cell variant of papillary
carcinoma present in a background of Hashimoto’s thyroiditis. Retrospective review of the FNA revealed a few clusters of follicular cells with
intranuclear inclusions indicative of papillary carcinoma. The illustrated
cells were originally interpreted as Hürthle cells (Diff-Quik, original magnification 11000).
Correlation between cytology and histology was
achieved in 73% of the diagnostic cases. The falsenegative rate of the ‘‘diagnostic’’ FNAs in our series
was 19% and the false-positive rate was 6%. The sensitivity and specificity were 80% and 94%, respectively.
The types of error made in our series were similar to
those reported in others.14 – 16 The difficulties in distinguishing between different types of follicular lesions
accounted for the largest group of cytodiagnostic errors and indeterminate diagnoses.
FNA is sensitive for the identification of papillary,
medullary, poorly differentiated follicular, and anaplastic carcinomas. However, its value is limited by its
inability to distinguish follicular lesions reliably. This
is predominantly due to overlapping cytologic criteria
among hyperplastic adenomatoid nodule in goiter, follicular adenoma, well-differentiated follicular carcinoma, and follicular variant of PC.7,14 – 22 The presence
of syncytial fragments and a microfollicular pattern
strongly suggests a follicular neoplasm; but in 15 – 25%
of cases, surgical resection will reveal a hyperplastic
nodule.23 – 25 Ravinsky and Safneck25 demonstrated that
follow-up of patients with smears displaying syncytialtype tissue fragments showed that 50% were from adenomas, 25% were from carcinomas, and 25% were
from nodular goiters.
The limitation of FNA in predicting the specific
histologic type of neoplasm, in particular distinguishing between follicular adenoma, follicular carcinoma,
and follicular variant of PC, has also been emphasized.
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257
Smears of the follicular variant of PC may yield monolayer sheets of uniform follicular cells with nuclear
grooves and intranuclear inclusions. However, these
characteristic features are not always present, and the
smears may display syncytial-type tissue fragments
with a follicular architectural pattern. As a result, this
tumor is often misinterpreted as a follicular neoplasm
or an adenomatoid nodule.26 – 29 In our series, four
cases of follicular variant of PC were misinterpreted
as adenomatoid nodules, four had indeterminate FNA
diagnoses, and one was misclassified as a follicular
neoplasm. Fortunately, the limitation of cytology in
distinguishing between follicular adenoma, follicular
carcinoma, and follicular variant of PC is not critical
from the standpoint of patient management, as the
generally accepted standard of treatment is to remove
a thyroid neoplasm surgically.8
The risk of malignancy with indeterminate cytology depends on the definition of the term and is reported as 15 – 20%.8,10 The current study demonstrated
that 77% (30 of 39) of the indeterminate cytologic diagnoses correlated with thyroid neoplasms histologically
(14 cases were benign [14 FAs] and 16 were malignant
[4 FCs, 7 PCs, 4 FVs, and 1 MC]). In comparison, 92%
of FNAs (37 of 40) originally reported as ‘‘diagnostic’’
of neoplasms correlated with neoplasms in the subsequent thyroidectomies (12 were FAs and 25 were malignant [22 PCs, 3 FCs]). Based on these results, it appears reasonable to consider patients with indeterminate FNA results for surgery. A previous study from
our department showed that a repeat FNA allowed
correct classification of 31% of thyroid nodules with
indeterminate diagnoses on the initial FNA.30 Suppressive therapy and repeat FNA are also advocated
for patients with indeterminate FNA results. Growth
of a nodule during suppressive therapy is considered
an indication for surgery. A study conducted by Frost
and Sidawy30 demonstrated that a lack of cytologic response to suppressive therapy does not confirm a neoplastic diagnosis because it can be observed in both
neoplastic and nonneoplastic nodules.
The reliability of the FNA procedure depends on
adequate cellularity of the smears, spreading the sample with minimal cellular damage, and preserving the
pattern of cellular distribution. Aspirates diluted with
blood, partially obscured by blood, or clotted are
sources of misinterpretation. Caraway et al9 noted that
false-negative cases could have been markedly reduced or eliminated if strict criteria for specimen adequacy had been applied. Proposed criteria for determining specimen adequacy varies slightly.8,17,31 – 34
Some authors require 5 – 6 groups of well-preserved,
well-visualized follicular cells, with each group containing 10 or more cells,31 whereas others require 8 –
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258
CANCER (CANCER CYTOPATHOLOGY) August 25, 1997 / Volume 81 / Number 4
10 fragments of well-preserved follicular cells on at
least 2 smears.17,34 However, it may be misleading to
adhere strictly to the definition of what constitutes
an adequate specimen. The evaluation of adequacy
remains subjective and is partially dependent on the
lesion and the experience of the pathologist. It may
be possible to establish a diagnosis of a classic PC
based on 6 clusters in one case, whereas 20 clusters
may be suboptimal in another. On the other hand, a
few spherules and honeycomb sheets of regular follicular cells in the presence of abundant, thick colloid
may be adequate for the diagnosis of an adenomatoid
nodule. The cellularity of all the FNAs included in the
current study met the minimum requirement of adequacy according to the published criteria; however,
retrospective evaluation of the discrepant cases
showed that 44% of the discrepancies were due to
samples of suboptimal quality. It is important to emphasize that the mere presence of an ‘‘adequate’’
number of well-visualized cells does not ensure adequacy. Difficult lesions may require more cellularity
to establish a correct diagnosis.
Despite its limitations, thyroid FNA remains a
powerful screening tool. In this series of 133 FNAs
obtained from patients who had subsequent thyroidectomies, 87 FNAs (65%) correlated with neoplasms
and 50 (38%) with malignant neoplasms. Of the 19
FNAs reported as follicular neoplasms, 15 cases correlated and 4 did not. Of the 4 discrepant cases, two
were PCs (1 usual and 1 follicular variant) and 2 were
adenomatoid nodules. Therefore, only 2 of the 19 cases
(10.5%) interpreted as follicular neoplasms cytologically did not correlate with a neoplasm. Therefore, the
probability that surgically treated lesions with an FNA
diagnosis of follicular neoplasm were indeed neoplastic was 89.5%. In addition, 13 of 25 errors in our discrepant category were not significant, i.e., 11 histologically proven follicular adenomas were interpreted as
adenomatoid nodules by FNA, an error of no particular
significance to the patient. Similarly, misclassifying
two histologically proven PCs (one usual and one follicular variant) as follicular neoplasms by FNA is not
an significant error because the cytology has identified
a lesion that required surgery.
features, particularly among hyperplastic adenomatoid nodules, follicular neoplasms, and follicular
variants of PCs.
j Rendering a definite diagnosis on a suboptimal FNA
sample that barely meets the proposed criteria for
adequacy may be a source of pitfalls.
j It is useful for the cytopathology laboratories to calculate the rates of neoplasms and malignancies in
indeterminate FNA cases. The knowledge of this data
may help clinicians determine the clinical management that is most appropriate for their patients.
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j Indeterminate FNA results and cytodiagnostic errors
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