Accuracy of Fine-Needle Aspiration of Thyroid
A Review of 6226 Cases and Correlation With Surgical or Clinical Outcome
Mojghan Amrikachi, MD; Ibrahim Ramzy, MD; Sheldon Rubenfeld, MD; Thomas M. Wheeler, MD
● Context.—Fine-needle aspiration has become an accepted and cost-effective procedure for rapid diagnosis of thyroid lesions. The routine use of fine-needle aspiration has
reduced the rate of unnecessary surgery for thyroid nodules.
Objectives.—To determine the accuracy of fine-needle
aspiration biopsy diagnosis and to discuss the possible pitfalls.
Design, Setting, and Participants.—Reports of 6226 fineneedle aspiration biopsies of the thyroid performed during
a period of 16 years (1982–1998) were reviewed. Computerized reports of the fine-needle aspiration biopsies
were sent to the physicians who performed the procedures,
and clinical follow-up information regarding the patients
was requested. Twenty-four clinicians participated in the
study. Histologic diagnoses were available for 354 cases.
The cytopathologic diagnoses were correlated with the histologic findings or clinical outcomes.
Results.—The cytologic diagnoses were as follows: 210
(3.4%) malignant, 450 (7.2%) suspicious, 3731 (60%) benign, and 1845 (29.5%) unsatisfactory. Most of the cases
with negative or unsatisfactory aspirates were followed
clinically or by repeat fine-needle aspiration. We identified
11 false-negative and 7 false-positive diagnoses. For aspirates considered sufficient for diagnosis, the sensitivity and
specificity levels were 93% and 96%, respectively.
Conclusions.—Fine-needle aspiration of the thyroid
gland is highly accurate and has a low rate of false-negative
and false-positive diagnoses. The major diagnostic problems are caused by diagnosis using a marginally adequate
specimen, diagnosis of malignancy based on just 1 or 2
atypical cytologic features, or overlapping cytologic features of follicular neoplasm with those of follicular variant
of papillary carcinoma.
(Arch Pathol Lab Med. 2001;125:484–488)
T
Fine-needle aspiration has made the surgical procedures much more selective, assisting in the treatment of
many patients. The routine use of FNA has reduced the
rate of unnecessary surgery for thyroid nodules and has
doubled the percentage of cancers found in the surgical
materials.4,5,10
Due to its simplicity, low cost, and absence of major
complications, this procedure is being performed on an
increasing number of patients, which has led to the detection of thyroid cancers at earlier stages, resulting in better
outcomes for patients. Nevertheless, like any other test,
FNA has its limitations. The reported pitfalls are those
related to specimen adequacy, sampling techniques, the
skill of the physician performing the aspiration, the experience of the pathologist interpreting the aspirate, and
overlapping cytologic features between benign and malignant follicular neoplasms.7,11,12
In this study, we reviewed the cytologic diagnoses of
more than 6000 consecutive FNA biopsies of the thyroid,
focusing on the correlation with surgical or clinical outcomes and possible pitfalls.
hyroid nodules are common clinical findings and have
a reported prevalence of 4% to 7% in the general population.1–3 Thyroid nodules are more common in women,
and the incidence increases with age, a history of radiation
exposure, and a diet containing goitrogenic material.3 The
vast majority of these nodules are nonneoplastic lesions or
benign neoplasms. However, the distinction of these benign lesions from a malignancy cannot be based reliably
on the clinical presentation only. Several diagnostic tests,
such as radionuclide scanning, high-resolution ultrasonography, and fine-needle aspiration (FNA) biopsy have been
used to select the patient population requiring surgical intervention. Recent studies have demonstrated that among
all these diagnostic modalities, FNA is the most accurate,
cost-effective, and simplest screening test for rapid diagnosis of thyroid nodules.4–6 Fine-needle aspiration has also
been shown to have similar or higher sensitivity and accuracy levels than frozen section examination.7–9
Accepted for publication November 7, 2000.
From the Departments of Pathology (Drs Amrikachi, Ramzy, and
Wheeler), Obstetrics-Gynecology (Dr Ramzy), Medicine (Dr Rubenfeld), and Urology (Dr Wheeler), Baylor College of Medicine, Houston,
Tex; and The Methodist Hospital, Houston, Tex (Drs Ramzy and Wheeler). Dr Amrikachi is now with the Department of Pathology, M. D.
Anderson Cancer Center, Houston, Tex.
Presented at the 88th Annual Meeting of the United States and Canadian Academy of Pathology, San Francisco, Calif, March 1999.
Reprints: Thomas M. Wheeler, MD, Department of Pathology, Baylor
College of Medicine, One Baylor Plaza, Houston, TX 77030 (e-mail:
twheeler@bcm.tmc.edu).
484 Arch Pathol Lab Med—Vol 125, April 2001
METHODS
The cytologic diagnoses of 6226 consecutive FNA biopsies of
thyroid performed on 4819 patients during a period of 16 years
(1982–1998) were reviewed. The data were obtained from the personal series of one of the authors (T.M.W.), at Baylor College of
Medicine, Houston, Tex. The procedures were performed by endocrinologists or surgeons, using 25-gauge needles. More than
20 clinicians contributed slides to the series; however, approxiFine-Needle Aspiration of Thyroid—Amrikachi et al
Figure 1. Cytologic diagnoses of 6226 fine-needle aspiration biopsies of thyroid.
Figure 2. Histologic diagnoses of 81 cases with a cytologic diagnosis of positive for papillary carcinoma.
Figure 3. Histologic diagnoses of 44 cases with a cytologic diagnosis of suspicious for papillary carcinoma.
Figure 4. Histologic diagnoses of 59 cases with a cytologic diagnosis of follicular neoplasm.
mately 50% of the procedures were performed by one of the authors (S.R.). The nodules were palpable and no ultrasound was
employed in the biopsy procedures.
An average of 6 to 10 spray-fixed smears were prepared and
sent to the cytology laboratory, where they were stained by the
Papanicolaou technique. Approximately 99% of the smears were
evaluated by the same pathologist (T.M.W.). The criteria used for
adequacy of specimens were those suggested by Kini et al13 and
included at least 6 to 8 tissue fragments of well-preserved follicular epithelium on each of 2 slides.
The cytology results were categorized into 4 groups: benign,
suspicious, malignant, and unsatisfactory. Aspirates classified as
‘‘benign’’ included adenomatous (colloid) nodule, Hashimoto thyroiditis, and subacute thyroiditis. The ‘‘suspicious’’ category included follicular neoplasm, Hürthle cell tumor, and aspirates
with atypical features suggestive of, but not diagnostic for, malignancy. The aspirates with unequivocal cytologic findings of
primary or secondary malignancy were classified in the ‘‘malignant’’ category. Aspirates with insufficient cellularity or poorquality smears due to delayed or inadequate fixation were considered ‘‘unsatisfactory.’’ This group also included the aspirates
consisting only of cyst fluid.
Computerized reports of the FNA biopsies were sent to the
clinicians who performed the procedures, and clinical follow-up
information regarding their patients was requested.
Histologic diagnoses were available for 354 (5.7%) cases. We
only had access to the pathology reports of the patients in whom
thyroidectomies were performed at outside institutions.
For statistical analysis, the cases with cytologic diagnoses of
positive or suspicious for malignancy, which on final histologic
examination were diagnosed as malignant, were considered true
Arch Pathol Lab Med—Vol 125, April 2001
positives. The cases with negative cytologic diagnoses that either
had a surgical specimen with benign diagnosis or a benign clinical course were considered to be true negatives. The false-positive category comprised the cases with a benign histology that
had a suspicious or positive cytologic diagnosis. A false-negative
diagnosis encompassed the cases with a malignant histology that
had been diagnosed as benign on cytology. We did not consider
papillary microcarcinomas as false negative when the much larger adjacent lesion was sampled and diagnosed appropriately.
Since unsatisfactory aspirates yielded no information, they were
excluded from calculations.
Sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of FNA relative to final histologic or
clinical outcome were calculated.
RESULTS
The cytologic diagnoses were as follows: 210 (3.4%) malignant, 450 (7.2%) suspicious, 3731 (60%) benign, and
1845 (29.5%) unsatisfactory (Figure 1).
The clinical follow-up interval ranged from 1 to 16
years. Approximately 13% of the cases with a negative
diagnosis and 29% of the cases with unsatisfactory aspirates were followed by repeat FNA.
Repeat FNA biopsies in 539 cases with initial diagnoses
of unsatisfactory provided diagnostic smears in 333 (62%)
cases. Of 495 patients with initial negative cytology who
had repeat FNAs, 4 (0.8%) were found to have malignant
aspirates.
Histologic diagnoses were available for 85 (40%) cases
Fine-Needle Aspiration of Thyroid—Amrikachi et al 485
Table 1. Number and Percentage of Cases With
Surgical Follow-up in Each Category
Cytologic
Diagnosis
No. of Cases
With Surgical
Follow-up, %
No. of
Cases, %
Malignant
Suspicious
Negative
Unsatisfactory
210
450
3731
1835
(3.4)
(7.2)
(60)
(29.5)
85
166
64
39
(40)
(36)
(1.7)
(2.2)
Table 2. Correlation of Cytologic and Histologic
Diagnoses
Surgical Diagnosis
Cytology
Diagnosis
Positive
Negative
Total
Positive
Suspicious
Negative
Unsatisfactory
Total
78
68
11
8
165
7
98
53
31
189
85
166
64
39
354
Table 3. Cytologic Diagnosis of 132 Cases With
Histologic Diagnosis of Papillary Carcinoma
Cytologic Diagnosis
No. (%) of Cases
Papillary carcinoma
Suspicious for papillary carcinoma
Suspicious NOS*
Suspicious for follicular carcinoma
Adenomatous nodule
Hashimoto thyroiditis
Unsatisfactory
Total
* NOS indicates not otherwise specified.
75
30
13
2
1
1
6
132
(57)
(23)
(10)
(2)
(1)
(1)
(5)
Table 4. Histologic Diagnoses of 28 Cases With
Cytologic Diagnosis of Hürthle Cell Neoplasm
Histologic Diagnosis
No. (%) of Cases
Hürthle cell adenoma
Follicular carcinoma
Hürthle cell carcinoma
Follicular adenoma
Adenomatous nodule
Total
13
7
2
3
3
28
(46)
(25)
(7)
(11)
(11)
with a cytologic diagnosis of positive for malignancy and
166 (36%) cases with a cytologic diagnosis of suspicious
for malignancy. Owing to referral to several other institutions, the results of surgical intervention were not available for the remaining cases. However, although this
group is relatively large (60%), no discrepancies between
cytologic and histologic diagnoses have been reported by
any of the treating physicians and no medicolegal consequences have emerged. Approximately 2% of the cases
with benign or unsatisfactory diagnoses were referred to
surgery (Table 1). Table 2 demonstrates the correlation of
cytologic and histologic diagnoses. For aspirates considered sufficient for diagnosis, the sensitivity and specificity
values were 93% and 96%, respectively. Positive predictive
values of cases with positive and suspicious cytologies
were 92% and 42%, respectively. Negative predictive value
of the cases with benign cytologic diagnoses was 99%,
with an accuracy of 96%.
The histologic findings for 81 patients with a cytologic
diagnosis of positive for papillary carcinoma and 44 cases
diagnosed as suspicious for papillary carcinoma are illustrated in Figures 2 and 3, respectively. Papillary carcinoma was found in 93% of the cases diagnosed as positive
for papillary carcinoma and 69% of the patients with a
cytologic diagnosis of suspicious for papillary carcinoma.
One patient in each group had follicular carcinoma. Conversely, on retrospective review of 132 cases with a histologic diagnosis of papillary carcinoma, 57% had a cytologic interpretation of positive for papillary carcinoma,
and 35% were suspicious for malignancy. In 6% of the
cases, the aspirates were nondiagnostic (Table 3).
Of 59 cases with the cytologic diagnosis of follicular
neoplasm, 11% had malignant histologic diagnoses. The
malignancies found in this group, in decreasing order of
frequency, were follicular carcinoma, medullary carcinoma, and papillary carcinoma. Eighty-one percent of the
cases were found to have follicular adenoma in the surgical specimen (Figure 4).
Histologic diagnoses of 28 patients with a cytologic diagnosis of Hürthle cell tumor are demonstrated in Table
4. Approximately 32% of these cases had malignancy on
subsequent surgical material.
We identified 7 cases with positive cytology diagnoses
who had benign lesions at surgery (Table 5). The most
common false-positive diagnosis was papillary carcinoma.
The cytology slides for 4 of these false-positive cases were
available for retrospective review. The smears of 3 cases
showed many cells with intranuclear inclusions and
grooves and occasional psammoma bodies, but they
lacked the other features of papillary carcinoma. The aspirates of the fourth case showed marked atypia; however,
due to scant cellularity, the smears were marginally adequate for optimal evaluation.
We had 11 false-negative diagnoses (Table 6). Retrospective review of the cytology slides for 7 of these cases
showed abundant colloid with benign follicular cells in 4
cases. In 3 cases, the specimens were marginally adequate
for appropriate evaluation.
Table 5. Histologic Diagnoses of 7 Cases With False-Positive Cytology
Cytology Diagnosis
Papillary carcinoma
Positive for malignancy, NOS*
* NOS indicates not otherwise specified.
486 Arch Pathol Lab Med—Vol 125, April 2001
Histologic Diagnosis
No. of Cases
Follicular adenoma 1 Hashimoto thyroiditis
Follicular adenoma
Multinodular goiter
Subacute granulomatous thyroiditis
Benign cystic nodule
Atypical adenoma
Hürthle cell adenoma
1
1
1
1
1
1
1
Fine-Needle Aspiration of Thyroid—Amrikachi et al
Table 6. Histologic Diagnoses of 11 Cases With False-Negative Cytology
Cytologic Diagnosis
Negative:
Negative:
Negative:
Negative:
Histologic Diagnosis
NOS*
follicular adenoma
Hashimoto thyroiditis
adenomatous nodule
No. of Cases
Papillary carcinoma
Well-differentiated follicular carcinoma
Follicular variant of papillary carcinoma
Follicular variant of papillary carcinoma
Hürthle cell carcinoma
Follicular carcinoma
5
1
1
2
1
1
* NOS indicates not otherwise specified.
Table 7. Comparing Our Data to Other Studies in the Literature
Series, y
Total No. of
Aspirates
Cytologic Diagnosis, %
Positive
Negative
Suspicious
Unsatisfactory Sensitivity, % Specificity, %
Gardiner et al, 1986
1465
1
74
10
Altavilla et al,16 1990
2433
1
78
5
Caraway et al,12 1993
394
17
60
14
Gharib et al,17 1993
10 971
4
64
11
Gharib,2 1993*
18 183
3.5
69
10
18
Burch et al, 1996
504
3
57
9
Baloch et al,7 1998
662
16
69
4
Current study
6226
3.4
60
7.2
* Review of 7 series.
† After repeat fine-needle aspiration biopsy, number of unsatisfactory diagnoses decreased to 22%.
15
COMMENT
In the last 20 years, FNA biopsy has evolved as the most
accurate and sensitive diagnostic tool for the initial screening of patients with thyroid nodules in the United
States.8,13,14 The ideal goal is to identify and surgically remove malignant nodules, while avoiding surgical intervention in benign lesions. In published series, the sensitivity
and specificity values of thyroid FNA vary from 65% to
98% and from 73% to 100%, respectively (Table 7).2,7,12,15–18
The main reason for such a wide range of sensitivity and
specificity is how cytopathologists handle the category of
‘‘suspicious’’ and how they define the false-positive and
false-negative results. Some authors include follicular lesion
in the malignant/neoplastic category. Others categorize
them in the negative group, whereas some exclude them
from the calculations altogether.2,7,12,15–18
In some series, the prevalence of malignancy in cases
with a cytologic diagnosis of suspicious for malignancy
approaches 60%.8 In our study, 41% of the cases with cytology classified as suspicious were found to have malignancy at surgery. The high percentage of malignancy in
cases with suspicious cytology justifies the need for surgical exploration of all cases in this category. However, in
cases with a cytologic diagnosis of malignancy, a more
extensive surgical intervention, such as total or near total
thyroidectomy, is the treatment of choice.8,9 Therefore, to
avoid a more aggressive surgical intervention with an increased risk of morbidity and mortality, definitive criteria
for the diagnosis of malignancy should be present before
a cytologic diagnosis of malignancy is considered.
In our review of 6226 thyroid FNAs, we identified 7
cases with false-positive cytology diagnoses. Of these cases, 3 underwent total thyroidectomy. The remaining 4 cases were treated more conservatively with thyroid lobectomy. The most common false-positive diagnosis was papillary carcinoma. The cytology slides for 4 of these falsepositive cases were available. These smears showed 1 or
more of the following characteristics: intranuclear incluArch Pathol Lab Med—Vol 125, April 2001
15
16
9
21
17
31
11
29†
65
71
93
98
83
80
92
93
91
100
91
99
92
73
84
96
sions, grooves, and occasional psammoma bodies. However, retrospectively, the other features of papillary carcinoma, such as finely granular chromatin, nucleoli, and
papillary or syncytial-type tissue fragments were absent.
One case showed marked atypia, but because of low cellularity, the smears were marginally adequate for optimal
evaluation. Retrospectively, these cases should have been
diagnosed as suspicious rather than positive for malignancy. The cytology and histology slides were not available in 3 of the false-positive cases. It is possible that the
surgical material were misinterpreted as benign in these
cases. Other investigators have reported a similar rate of
false-positive diagnosis. Kini13 reported a 3% rate of falsepositive diagnosis in a series of 316 patients with a cytodiagnosis of papillary carcinoma. In that study, most often
the errors were due to interpretation based on insufficient
criteria, especially in a very cellular aspirate with degeneration and papillary formation.
Since FNA is considered as a screening tool for patients
with a thyroid nodule, a 2% false-positive rate is not of
major concern. However, the goal is to decrease the rate
of false-negative diagnosis. In our study, we identified 11
false-negative diagnoses. The cytology slides were available for 7 cases in this group. Retrospective review of the
smears for 4 of these cases showed abundant colloid with
benign follicular cells and no evidence of neoplastic
changes. Since no ultrasound guidance was used during
these procedures, some of these false-negative results
could be due to sampling errors. The interval between the
initial negative diagnosis and the surgery was several
years in some cases. Therefore, the possibility of development of new malignancy in a previously benign lesion
should also be considered. In the other 3 cases, the specimens were marginally adequate for appropriate evaluation and probably should have been classified as unsatisfactory rather than negative.
The reported rates of false-negative cytology diagnoses
range from 1% to 16% in different series.2,7,12,15–18 The high
Fine-Needle Aspiration of Thyroid—Amrikachi et al 487
false-negative rate in some of these reports is because
these studies were often conducted as retrospective investigations of patients with thyroidectomy with only subsequent review of the cytologic material. Thus, the large
number of patients with a negative cytologic diagnosis
who did not undergo surgery because of the negative FNA
results was not included in their statistical analyses. Indeed, in our series, had we used such criteria, our falsenegative rate would have been 17% (11/64).
Very few investigators have addressed the clinical follow-up data. Grant et al14 studied the accuracy of thyroid
FNA-based diagnosis, particularly with respect to falsenegative errors, in a group of 680 patients with a mean
follow-up period of 6.1 years. They reported less than 1%
false-negative diagnoses for 439 patients with a negative
cytodiagnosis and no false-positive diagnoses for 24 cases
with positive cytology.14 In our study, we correlated the
cytology results with the surgical pathology diagnosis, repeat FNA, or clinical follow-up information. Of 3731 aspirates with negative cytologic diagnoses, 64 patients (2%)
with clinically suspicious nodules underwent surgical exploration. Of these, 11 patients were found to have malignant lesions at surgery. Repeat FNA in 495 cases with an
initial negative cytology showed malignancy in only 4
(0.8%). The remaining cases had close follow-up, ranging
from 1 to 16 years, and no discrepancies were reported
by the treating physicians. Therefore, the overall false-negative rate in our study was less than 1%. Some cases in
our study may have been lost to follow-up, or low-grade
malignancies may have been clinically stable. However,
due to the large number of negative cases with clinically
benign follow-up, we believe that our true-negative rate is
very close to the actual figure.
One of the major limitations of FNA of the thyroid is
the large number of insufficient aspirates. Insufficiency
rates ranging between 7% and 31% have been reported
(Table 7).12,15–18 The most important factors in the rate of
insufficient aspirates are the experience of the aspirator
and the criteria used to define a satisfactory specimen.7,18
In our study, the insufficiency rate was 29%, and that was
reduced to 22% after repeat FNAs were performed. Although this insufficiency rate seems to be on the high side
of the previous reports, all procedures in this study were
performed by clinicians, without adequacy checks at the
time of the aspiration. In addition, some of palpable nodules were due to cystic lesions that yielded fluid with
mostly histiocytes and few if any follicular cells, which
did not meet the criteria proposed for an adequate sample.
Recently, the Papanicolaou Society of Cytopathology published guidelines for the examination of FNA specimens
from thyroid nodules. They suggest reporting such cases
as ‘‘consistent with benign thyroid cyst,’’ with a qualifier
indicating that the interpretation is limited by paucity or
lack of follicular cells, rather than reporting them as insufficient for diagnosis.19 Most of the cases with insufficient aspirates in our series were followed clinically or by
repeat FNA. Of 539 cases with initial insufficient aspirate
classifications, 62% had a diagnostic aspirate after repeat
FNA. Some series have reported on the accuracy of thyroid FNA biopsy over time. Our study did not address
this point.
In summary, FNA of thyroid is highly accurate and has
488 Arch Pathol Lab Med—Vol 125, April 2001
a low rate of false-negative and false-positive diagnoses.
If the suspicious diagnoses are considered positive (because these patients were also sent to surgery), the sensitivity and specificity values of thyroid FNA are 93% and
96%, respectively. Fine-needle aspiration of the thyroid is
highly specific in the diagnosis of most of the benign lesions, such as adenomatous nodules and lymphocytic thyroiditis, and in several malignant conditions as well, such
as papillary carcinoma and anaplastic carcinoma. Although the cytologic diagnosis of papillary carcinoma has
the highest specificity of thyroid malignancies, the most
common false-positive diagnosis is also papillary carcinoma. Cytopathologists should be aware of these potential
limitations of FNA interpretation. The major diagnostic
problems arise when a marginally adequate specimen is
interpreted in a definitive fashion or when the diagnosis
of malignancy is made based on just 1 or 2 atypical cytologic features. Overlapping cytologic features of follicular neoplasm with those of follicular variant of papillary
carcinoma is another diagnostic challenge. Patients with
benign cytologic findings should have close clinical follow-up. There is a possibility of false-negative diagnosis
in a small percentage of patients. Therefore, despite a benign cytology, clinically suspicious lesions probably
should be excised if the patient is a surgical candidate.
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