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CANCER
299
CYTOPATHOLOGY
Ultrasound-Guided Fine-Needle Aspiration
Biopsy of the Thyroid
Rosemary Tambouret, M.D.
Wanda M. Szyfelbein, M.D.
Martha B. Pitman, M.D.
BACKGROUND. We reviewed the Massachusetts General Hospital experience with
Department of Pathology, Massachusetts General
Hospital, Boston, Massachusetts.
METHODS. All radiologically guided FNABs of the thyroid from January 1993
ultrasound-guided fine-needle aspiration biopsies (FNABs) of the thyroid to determine the indications, rate of unsatisfactory smears, correlation with excisional
biopsy results, and verification of efficient use of personnel time.
through June 1997 were reviewed. As a measure of efficient use of technologist
time, a sample of times spent by the technologist during the procedure for 20 cases
in 1993 and 1997 was compared with that of an equal number of random nonthyroid image guided FNABs.
RESULTS. Two hundred-ninety FNABs were identified in 251 patients, representing 12% of all thyroid FNABs and 11% of all radiologically guided FNABs.
Indications in the 251 patients included multiple nodules (78), solitary nodules
(61), complex nodules (39), prior failed FNAB (39), thyroid bed abnormalities
post-thyroidectomy (21), difficult access (7), and investigation of recurrent
tumor in residual thyroid lobe (6). Available records indicated 118 lesions were
palpable and 45 were nonpalpable; the physical examination characteristics of
the remainder (88) were not stated. Diagnoses included 44 unsatisfactory cases
(15%), 103 macrofollicular lesions, 20 microfollicular lesions, 26 mixed macro/
microfollicular lesions, 5 oxyphilic lesions, 1 trabecular pattern, 15 nonspecific
follicular cell pattern, 9 follicular cell atypia, 30 cysts, 11 thyroiditis, 23 malignant tumors, and 3 other (1 parathyroid, 2 lymph node). Eighty-nine FNABs
from 76 patients had subsequent surgical biopsy. Excisional biopsies in 14
unsatisfactory FNABs were benign. In the remaining 75 FNABs from 67 patients,
18 malignancies on FNAB were correctly diagnosed, but 3 other papillary
carcinomas were only qualified as atypical follicular cells on cytology. No
false-positive cases occurred. Of 15 macrofollicular lesions on cytology, 10 were
adenomas on excision, only 2 of which were microfollicular adenomas, and 4
were adenomatous nodules. An aspirate of a parathyroid adenoma was misinterpreted as a macrofollicular lesion of the thyroid. Three microfollicular lesions on FNAB proved to be nodular hyperplasia on excision, and the other 11
were adenomas, 5 of them microfollicular. Average technologist time was
significantly longer for thyroid FNABs than nonthyroid FNABs in 1993, but in
the 1997 sample no significant difference was identified.
CONCLUSIONS. Radiologically guided FNAB of the thyroid is a clinically useful
Presented in abstract form at the 87th Annual
Meeting of the United States and Canadian Academy of Pathology, Boston, MA, March, 1998.
procedure with a high correlation between benign lesions not needing excision
(macrofollicular), and lesions that need excision (microfollicular/oxyphilic cell
or malignant). Technologist time needed for immediate evaluation tends to
Address for correspondence: Rosemary Tambouret, M.D., Department of Pathology, Massachusetts General Hospital, 55 Fruit Street, Boston, MA
02114.
decrease with increasing operator experience. Cancer (Cancer Cytopathol)
Received December 31, 1998; revision received
April 21, 1999; accepted April 28, 1999.
KEYWORDS: thyroid, parathyroid, cytology, ultrasound-guided fine-needle aspiration biopsy.
© 1999 American Cancer Society
1999;87:299 –305. © 1999 American Cancer Society.
300
CANCER (CANCER CYTOPATHOLOGY) October 25, 1999 / Volume 87 / Number 5
hyroid nodularity is a frequent clinical problem.1,2
Although the estimated risk of developing a palpable thyroid nodule is 5 to 10%,3 autopsy and ultrasound studies of individuals with clinically normal
thyroids have demonstrated the presence of nodules
in 25 to 40% of cases.4 –10 However, only 5 to 15% of
surgically excised nodules prove to be malignant.
Fine-needle aspiration biopsy (FNAB) has become a
standard initial step in the work-up of thyroid nodules, although protocols for the triage of thyroid lesions vary somewhat from one institution to another.
The goal of the procedure is to identify for excision
clinically significant lesions, either malignant or with
the potential for malignancy, and observe all others. At
our institution, most thyroid FNABs are performed by
a clinician or cytopathologist on palpable masses (approximately 700 per year). In certain cases, however,
such as a nonpalpable mass discovered by radiological
techniques during surveillance of patients at high risk
for thyroid cancer or during radiological study of
nearby structures (e.g., the carotid artery), real-time
imaging studies guide the procedure, which aids in
obtaining adequate material.11,12 A radiologist performs ultrasound (US)-guided thyroid FNABs with immediate evaluation by a cytotechnologist and a cytopathologist to ascertain adequacy, a procedure that
demands considerable personnel time. In addition,
because US-guided FNAB of the thyroid is perceived
by our cytology staff as frequently yielding suboptimal
or nondiagnostic results while being excessively time
consuming, we undertook a review of the Massachusetts General Hospital (MGH) experience to determine
the indications, rate of unsatisfactory smears, and correlation with subsequent biopsy diagnosis. We also
wished to evaluate whether the technologist’s time
was being efficiently used in preparing and staining
smears for rapid interpretation.
T
METHODS
Pathology and clinical records were reviewed on all
cases of radiologically guided FNABs of the thyroid
from January 1993 through June 1997, for indication,
clinical history, cytological diagnosis, and histological
follow-up. An individual FNAB was defined as the
ensemble of samples or passes taken from one lesion
in a patient at one specific time. The data were compared with the number of all thyroid FNABs and with
all radiologically guided FNABs performed during the
same period.
The FNABs were obtained by a radiologist, freehand, under continuous real-time sonographic guidance with 7- to 10-MHz high-frequency transducers.
The patient was supine with neck extended. With the
operator at the patient’s head, the neck was trans-
versely scanned, the lesion was located, and local anesthetic was administered adjacent to the medial or
lateral edge of the transducer. Needle size generally
ranged from 22 to 25 gauge, although rarely an 18- or
20-gauge needle was used, and 1 mL of suction was
applied. The exact number of passes varied from 1 to
12, but frequently the radiologist simply noted that
multiple samples had been obtained from the lesion.
Adequacy was determined during the procedure by a
cytotechnologist who made smears and immediately
fixed the smears in 95% alcohol. Smears for rapid
interpretation were stained with hematoxylin and
eosin. The cytotechnologist and the pathologist determined if the sampling was adequate or if additional
sampling was advised. The remainder of the alcoholfixed smears were later Papanicolaou stained. Needle
rinsings were evaluated and submitted for cytological
preparation (Cytospin or ThinPrept) or for cell block if
tissue fragments were visible.
Cytological reports contained a statement of adequacy and a cytological diagnosis. Adequacy was designated as “unsatisfactory,” “satisfactory but limited
by . . . [reason],” and “satisfactory” according to the
judgment of the individual cytopathologist; uniform
guidelines were not used. For the cases of “satisfactory
but limited by . . . ,” the slides were reviewed, and the
number of cell groups present were tabulated to compare with published guidelines for adequacy.13–15 The
cases were divided into three groups: 1) 10 or more
groups per case with 20 or more cells per group, 2) 6 or
more groups per case with 10 to 20 cells per group,
and 3) 0 to 9 groups of 10 or more cells per group.
The main cytological diagnoses of the thyroid included follicular lesions, subdivided into macrofollicular, microfollicular, mixed macro/microfollicular,
and nonspecific types. Macrofollicular lesions are
those exhibiting more than 90% of their cells as groups
or sheets of at least 6 to 12 uniform, round, nonoverlapping follicular cells in a background of colloid or
cyst debris. A microfollicular lesion is composed predominantly of small groups of few follicular cells in a
ring or rosette arrangement. A mixed lesion contains
variable proportions of microfollicles and macrofollicles. This categorization is intended to give an estimate of the risk that a given lesion is follicular carcinoma. For example, a macrofollicular lesion—whether
a colloid nodule, an adenomatous nodule of nodular
goiter, or a macrofollicular adenoma— has almost no
risk of malignancy, whereas a microfollicular lesion is
likely to be neoplastic and carries a risk of approximately 20 to 25% of being a follicular carcinoma,
somewhat higher or lower depending on the presence
or absence of associated risk factors.3,16
An estimate of technologist’s time needed during
US-Guided FNAB Thyroid/Tambouret et al.
TABLE 1
Indications for Radiologically Guided Biopsy
301
TABLE 2
Unsatisfactory Cases
Indication
Number of patients
Multiple nodules
Solitary nodule
Prior failed FNAB
Complex nodules
Thyroid bed abnormality post-thyroidectomy
Difficult access
Recurrent carcinoma in residual lobe of thyroid
Total patients
78 (31.4%)
61 (24.1%)
39 (15.5%)
39 (15.5%)
21 (8.3%)
7 (2.8%)
6 (2.4%)
251 (100%)
the procedure was obtained by averaging the time
spent by the technologist at the FNAB from 20 consecutive US-guided thyroid FNABs in 1993 and 20 in
1997, compared with similarly selected nonthyroid
FNABs. Student t-test was used to compare the two
groups.
RESULTS
Patient Demographics
The study population consisted of 290 FNABs in 251
patients (79 men and 172 women) aged 17 to 85 years
(average 52.3 years), constituting 12% of all thyroid
FNABs and 11% of all radiologically guided FNABs
performed during this time period.
Two hundred sixteen patients had one FNAB, 31
patients had two FNABs (25 synchronously of different
lesions in the thyroid and 6 metachronously of the
same lesion), and 4 patients had three FNABs, all at
the same time of three separate thyroid lesions.
The lesion size, recorded in 113 FNABs in 100
patients (43%), ranged from 0.3 to 4 cm (1.8 cm average); 17 were less than 1 cm in diameter. The lesion
type was a solitary nodule in 122 patients, multiple
nodules in 108 patients, and a thyroid bed lesion postthyroidectomy in 21 patients.
The indications for use of US guidance (Table 1),
other than the simple presence of a solitary nodule in
61 patients, included multiple nodules (78), complex
nodules (39), prior failed FNAB performed without
guidance (39), thyroid bed abnormalities post-thyroidectomy (21), difficult access (7), and abnormalities
in a residual thyroid lobe worrisome for recurrent
carcinoma (6). Examples of difficult access included
substernal dominant nodules in a multinodular goiter
and nodules near large vessels.
Palpable masses or diffuse glandular enlargements were noted in 118 glands. Nonpalpable lesions
were found in 45 glands, and the quality of the remainder (88) on physical examination could not be
determined from the records examined.
Thirteen lesions were found incidentally during
Total
Too few follicular cells
Excision or biopsy (n 5 11)
Mixed adenoma
Microfollicular adenoma
Follicular adenoma, NOS
Macrofollicular lesion, NOS
Hashimoto’s thyroiditis
Thyroid bed fibrosis
No follicular cells or colloid
Excision or biopsy (n 5 2)
Benign thyroid tissue, NOS
Thyroid bed fibrosis
Colloid or debris only
Excision (n 5 1)
Benign thyroid tissue
N 5 44 (15%)
29 (65%)
6
1
1
1
1
1
9 (20%)
1
1
6 (14%)
1
NOS: not otherwise specified.
scans of other sites, such as a carotid or parathyroid
scan. Of the 13 incidental lesions, 8 were solitary with
all but 1 nonpalpable. Five glands contained multiple
nodules. Size was recorded in four and ranged from 1
to 3 cm. Ultrasound follow-up post-FNAB of the incidental lesions in two patients demonstrated a decrease in the size of the nodules. Five patients had no
further recorded follow-up, and six had excisions revealing benign lesions except for one papillary carcinoma.
Sixty patients had one or more significant associated clinical conditions, including prior radiation
therapy (27), prior history of thyroid carcinoma (26),
carcinoma at other sites (10), and a family history of
medullary carcinoma (1).
Cytological Diagnoses
Initially, 49 cases were categorized as unsatisfactory;
however, 5 had accompanying adequate cell blocks, 2
of which showed a microfollicular lesion, 1 a macrofollicular lesion, and 2 a nonspecific follicular pattern.
Excluding the cases with adequate cell block, 44
cases were truly unsatisfactory (15%) (Table 2). Of
these, five were FNABs of the thyroid bed, post-thyroidectomy (for medullary carcinoma in one case and
papillary carcinoma in four cases) and were all
deemed unsatisfactory because of absent or too few
cells.
Of the remaining 39 unsatisfactory cases, 11 samples
were from 7 patients who had multiple sites sampled
during the procedure. In five of the seven patients, one
or more samples were adequate. Inadequate smears
were obtained in 25% of patients having multiple sites
aspirated, as opposed to only 14.8% of those undergoing
302
CANCER (CANCER CYTOPATHOLOGY) October 25, 1999 / Volume 87 / Number 5
TABLE 3
Satisfactory FNABs in 246 Patients*
Histology
Cytological findings
Follicular adenomas
Follow-up biopsy
Total
246
FNABs
N 75
(30.6%)
NOS
Micro
Mixed
Adenomatous
nodule
Macro
Micro
Mixed
Nonsp foll patt
Oxy
Atyp foll cells
Trab
Coll nod/cyst
Ch thy/Hashi
Pap ca
Med ca
Anapl ca
LN
Parath
Totals
103
20
26
15
5
9
1
30
11
20
2
1
2
1
(41.9%)
(8.1%)
(10.6%)
(6.1%)
(2.0%)
(3.6%)
(0.4%)
(12.2%)
(4.5%)
(8.1%)
(0.8%)
(0.4%)
(0.8%)
(0.4%)
15
14
10
0
2
9
1
4
1
16
1
1
0
1
75
(14.7%)
(70%)
(38%)
(0%)
(40%)
(100%)
(100%)
(13%)
(9%)
(80%)
(50%)
(100%)
(0%)
(100%)
5
4
2
5
3
2
2
4
3
5
1
1
1
1
3
1
1
2
Benign
NOS
Diffuse
hyperplasia
Pap
ca
Med
ca
Ana
ca
Parath
1
2
1
3
2
16
1
1
27
7
14
2
1
19
1
1
1
2
* Including 5 by cell block only and 36 “evaluation limited by . . .”.
Macro: macrofollicular lesion; Micro: microfollicular lesion; Mixed: mixed follicular lesion; Nonsp foll patt: nonspecific follicular pattern; Oxy: oxyphilic lesion; Atyp foll cells: atypical follicular cells; Trab: trabecular
lesion; Coll nod: colloid nodule; Ch thy/Hashi: chronic thyroiditis, Hashimoto’s disease; Pap ca: papillary carcinoma; Med ca: medullary carcinoma; Ana ca: anaplastic carcinoma; LN: lymph node; Parath: parathyroid;
NOS: not otherwise specified.
an FNAB of a single site; multiple site samples seemed to
predispose to more unsatisfactory specimens.
Out of the 246 satisfactory cases (241 on cytology
and 5 on cell block alone), the evaluation of 36 was
limited by various factors, including obscuring blood;
obscuring chronic inflammation; lack of follicular architecture, with single follicular cells predominating;
or few to no follicular cells. Size was noted in 11 of
these 36 cases: 2 were 1 cm, 4 were 1 to 2 cm, and 5
were more than 2 cm. Five of the paucicellular cases
were consistent with cysts. Slides were available in 29
of the 36 cases. On review of these 29 cases, 11 had at
least 10 well formed follicular groups (up to 54), with
more than 20 cells per group. Fifteen cases had 6 to 40
groups of follicular cells with each group containing
10 to 20 cells, as well as lesser numbers (0 to 9) of
groups with more than 20 cells. Finally, three cases
had 0 to 6 cell groups of more than 10 cells/groups,
and their diagnoses included two cysts, one of which
had no follicular cell groups and one with only three
cell groups. The third consisted of a vast amount of
lymphocytes but only two groups of follicular cells,
consistent with chronic thyroiditis. Thus, depending
on which of the published guidelines were used, either
11 of 29 cases (33%) or 26 of 29 (90%) were fully
adequate.
The cytological diagnoses of the 246 fully satisfactory cases (by cytology or cell block) are listed in Table
3. A macrofollicular lesion was the most common
diagnosis, rendered in 103 FNABs (41.9%). Microfollicular or mixed follicular patterns were identified in
46 FNABs. Nonspecific or atypical follicular cells were
found in 24 FNABs (10%), and 5 FNABs (2%) contained
predominantly oxyphilic cells. Colloid cysts or nodules
were recognized in 30 FNABs (12.2%). Twenty-three
FNABs (9.3%) were diagnosed as malignant and included papillary carcinoma (20), medullary carcinoma
(2), and anaplastic carcinoma (1). Two lymph nodes
and one parathyroid gland were diagnosed as such on
FNAB; however, another FNAB was recognized to be
from the parathyroid gland only on retrospective review.
Follow-Up Excisional Biopsies
Seventy-six (30%) patients with 89 FNABs had subsequent surgical excision or biopsy. However, 14 of the
89 FNABs were unsatisfactory, leaving 75 FNABs for
correlation. Follow-up excision in the 14 unsatisfactory FNABs were all benign (Table 2). In three of the
five unsatisfactory thyroid bed aspirates, only fibrosis
was identified on excisional biopsy, which correlated
with the absent or scant cellularity seen on FNAB.
Of the 246 satisfactory FNABs, 75 had tissue follow-up in 67 patients (Table 3). In 75% of the excisions
neoplasms were found, 30% of which were malignant.
Included in this group were lobectomies in two pa-
US-Guided FNAB Thyroid/Tambouret et al.
tients after FNABs in which only the cell blocks were
adequate, showing a microfollicular pattern. Histology
in both cases identified microfollicular adenomas.
Also included in this group were six surgical biopsies
in the group of 36 cases characterized as “evaluation
limited by . . .”. All six biopsy samples were benign,
including two follicular adenomas and one adenomatous nodule. The cytological diagnoses in these three
cases had been macrofollicular lesion, mixed follicular
lesion, and atypical follicular cells. No false-positive
cases occurred.
Three cases of papillary carcinoma were given
only descriptive diagnoses noting the presence of
atypical follicular cells with various abnormal features
such as excessive nuclear grooves. One of these cases
was a part of a pair of FNAs, the second of which was
diagnostic of papillary carcinoma.
Of follicular lesions, those qualified as macrofollicular and nonspecific follicular pattern tended to be
excised less frequently (14.7% and 0%, respectively)
than those identified as mixed follicular or microfollicular lesions (38% and 70%, respectively). Similarly,
the diagnosis of an oxyphilic, trabecular, or atypical
follicular lesion often was followed by excision (80%).
Of those designated macrofollicular on cytology, 2 of
15 (13%) were microfollicular adenoma on excision as
opposed to 5 of 14 (36%) microfollicular lesions. None
of the mixed macro/microfollicular lesions proved to
be microfollicular adenomas on excision. No follicular
carcinoma was identified.
The unrecognized parathyroid FNA was from a
1-cm, palpable cystic nodule in the right lower pole of
the thyroid in a 44-year-old euthyroid female. A macrofollicular lesion was diagnosed cytologically. When
removed, the nodule was found to be a parathyroid
adenoma. The patient’s serum calcium level, which
had been 10.2 mg/dL preoperatively, decreased to 8.3
mg/dL immediately postoperatively. Serum parathyroid hormone level had not been obtained because the
adenoma was an unexpected finding. Review of the
cytologic smears showed a low to moderately cellular
sample composed predominantly of naked nuclei and
few cells in groups with abundant delicate to oncocytic cytoplasm. The nuclei showed moderate anisonucleosis, chromatin stippling, and nuclear overlap.
Microacini were identifiable, as were fragments of
capillaries. Rare histiocytes were seen.
The negative predictive value of a cytological diagnosis of a macrofollicular or mixed follicular lesion—that is, the ability to predict lesions that need
not be excised (adenomatous nodules, macrofollicular
and mixed follicular adenomas)—was 88%.
The positive predictive value of a cytological diagnosis of microfollicular lesion, oxyphilic lesion, or le-
303
TABLE 4
Technologist Time in Performing FNAB
Procedure
1993
average
1997
average
Overall
average
P value
Thyroid FNAB
Nonthyroid FNAB
74 min
57 min
66 min
58 min
70 min
57 min
0.0319
0.1435
sion with atypical follicular cells or malignant cells—
that is, the ability to predict lesions that need to be
excised (microfollicular adenoma and thyroid carcinoma)—was 65%.
Technologist Time
On average, the technologist time for US-guided thyroid FNAs was 70 minutes (74 minutes in 1993 and 66
minutes in 1997), whereas for other radiologically
guided FNABs, the average time was 57 minutes (57
minutes in 1993 and 58 minutes in 1997).
The difference in time for thyroid FNABs as opposed to other radiologically guided FNABs was significantly different for the 1993 group (P 5 0.0319) but
not for the 1997 group (P 5 0.1435), (Table 4). This
may reflect a learning curve for the radiologist or
simply a difference in personnel.
DISCUSSION
Although most FNABs of the thyroid can be accomplished without US localization, in certain situations
image guidance may be necessary. Indications for US
include indeterminate physical examination, nonpalpable lesions identified in patients at high risk for
thyroid malignancies, and prior failed or nondiagnostic FNAB using direct palpation.17 In one series, about
50% of nondiagnostic FNABs without guidance were
caused by cyst contents only, and subsequent repeat
FNAB under US guidance helped correctly place the
needle in the solid portion of the mass.18 Nondiagnostic FNABs are associated with thyroid malignancy in
an estimated 2 to 9% of cases.19 –21 The percentage is
greater in high-risk categories such as in men, in those
exposed to radiation, and in those with larger nodules.
Recent studies have questioned the utility of FNAB in
small nonpalpable masses (less than 1.5 cm) because
small masses, even if malignant, rarely cause clinical
disease.22,23 Review of our material showed only 5.2%
of US-guided FNABs were performed on lesions identified incidentally during scans of other sites. The majority were performed for reasons of difficult access,
complexity, multiplicity of nodules, prior failed FNAB,
or investigation of possible recurrent carcinoma.
Our 15% unsatisfactory rate is at the limit of the
304
CANCER (CANCER CYTOPATHOLOGY) October 25, 1999 / Volume 87 / Number 5
acceptible range advised by the Papanicolaou Society Guidelines,13 which suggest less than 15% for the
unsatisfactory rate and, although borderline, is
heartening in view of the impression of poor performance held within the department. Cochand-Priollet et al.24 reported an unsatisfactory rate of only
3.8% in their group of US-guided thyroid FNABs, but
all their cases were palpable masses. Our cases
deemed “satisfactory but limited by . . .” were surprisingly cellular. By applying the broader published
guidelines, only 3 of 29 cases were limited by scant
cellularity. Thus, US per se does not seem to engender less than optimal smears.
This review also demonstrated the usefulness of
our terminology regarding follicular lesions. Microfollicular adenomas were found more frequently after cytological diagnosis of a microfollicular lesion
than after diagnosis of a macrofollicular or mixed
lesion. This terminology may be more clinically useful than attempting to employ the surgical pathology diagnostic categories for follicular lesions in
cytology specimens because overlap exists in their
use in cytology.25
A well recognized pitfall in interpretation of aspirates from the region of the thyroid gland is failure to
consider the possibility of a parathyroid lesion unless
suspicion is raised by the clinical information.26 Features that are found in FNABs of parathyroid adenoma
and that were present in our case included nuclear
chromatin stippling; delicate, clear, or granular cytoplasm easily stripped from cells, leaving naked nuclei;
nuclear overlap; three-dimensional clusters; and microacini.27,28 Although a helpful clue is perivascular
cell arrangement, only rare capillaries without clinging
epithelial cells were seen in our case.
Finally, with experience, technologist time does
not seem to be significantly longer for thyroid FNAB
compared with FNAB of other body sites. In conclusion, US guidance is useful for certain types of thyroid
nodules. At our institution, US guidance of the thyroid
is employed for a variety of situations. Only a limited
number of incidental nodules are aspirated, in accordance with published recommendations.
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