Neuroradiolog y / Head and Neck Imaging • Original Research

Bonavita et al.
Thyroid Ultrasound

Neuroradiology/Head and Neck Imaging

Original Research

Pattern Recognition of Benign

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Nodules at Ultrasound of the

Thyroid: Which Nodules Can
Be Left Alone?
John A. Bonavita1 OBJECTIVE. The purpose of this study was to evaluate morphologic features predictive
Jason Mayo1 of benign thyroid nodules.
James Babb1 MATERIALS AND METHODS. From a registry of the records of 1,232 fine-needle
Genevieve Bennett 1 aspiration biopsies performed jointly by the cytology and radiology departments at a single
Thaira Oweity 2 institution between 2005 and 2007, the cases of 650 patients were identified for whom both
a pathology report and ultrasound images were available. From the alphabetized list gener-
Michael Macari1
ated, the first 500 nodules were reviewed. We analyzed the accuracy of individual sonograph-
Joseph Yee1 ic features and of 10 discrete recognizable morphologic patterns in the prediction of benign
Bonavita JA, Mayo J, Babb J, et al. histologic findings.
RESULTS. We found that grouping of thyroid nodules into reproducible patterns of mor-
phology, or pattern recognition, rather than analysis of individual sonographic features, was
extremely accurate in the identification of benign nodules. Four specific patterns were identi-
fied: spongiform configuration, cyst with colloid clot, giraffe pattern, and diffuse hyperecho-
genicity, which had a 100% specificity for benignity. In our series, identification of nodules
with one of these four patterns could have obviated more than 60% of thyroid biopsies.
CONCLUSION. Recognition of specific morphologic patterns is an accurate method of
identifying benign thyroid nodules that do not require cytologic evaluation. Use of this ap-
proach may substantially decrease the number of unnecessary biopsy procedures.

Keywords: fine-needle aspiration, nodule, thyroid,
ultrasound
DOI:10.2214/AJR.08.1820
Received September 12, 2008; accepted after revision
October 24, 2008.
1 ing a rapid transition from nuclear medicine
Department of Radiology, Langone Medical Center, New
York University School of Medicine, 550 First Ave., New
York, NY 10016. Address correspondence to J. Bonavita
(john.bonavita@nyumc.org).
2
Department of Pathology, Langone Medical Center, New
York University School of Medicine, New York, NY.
AJR 2009; 193:207–213
0361–803X/09/1931–207
© American Roentgen Ray Society
O
ne of the consequences of in-
creased use of imaging has been
the discovery of incidentalomas,
or pseudodiseases, that are com-
mon in the general population but have no or
minor clinical significance. Once such inci-
dentaloma, the thyroid nodule, is extremely
common, found in some autopsy series in as
much as 50% of the general population [1,
2]. Most of these nodules are benign; the in-
cidence of malignancy is quite low, 3–7%
[3–5]. In the late 1990s, articles began to ap-
pear questioning the reliability of radiotracer
uptake as a predictor of benignity, occasion-
to ultrasound for evaluation of the thyroid
[6–8]. The superior resolution of ultrasound
images has resulted in discovery of a large
number of thyroid nodules that heretofore
had been obscured [9].
Since the late 1990s, several studies have
been conducted to analyze the relation be-
tween specific sonographic features of thy-
roid nodules and malignancy [2, 10–16]. Al-
though guidelines have been established,
such as those of the Society of Radiologists in
Ultrasound, the American Thyroid Associa-
tion, and the European Thyroid Association
[2, 17–22], they are commonly confusing and
at times ignored in everyday practice, largely
because of lack of familiarity with and trust
in their validity. Common in the studies is
a persistent limitation of specificity and sen-
sitivity of specific ultrasound features in the
prediction of malignancy. Some authors [23,
24] advocate a changed approach of recogni-
tion of specific patterns rather than individ-
ual ultrasound features in separation of nod-
ules that require biopsy from those that do
not. The purpose of our study was to evaluate
the accuracy of such a morphologic feature–
oriented approach to the identification of be-
nign thyroid nodules.
Materials and Methods
Patients
Among the records of 1,232 fine-needle aspir­
ation (FNA) biopsies performed jointly by the
cytology and radiology departments at a single
institution from January 2005 to December

AJR:193, July 2009 207

 Bonavita et al.

2007, the cases of 650 patients (436 women, 64
men; average age, 54.7 years; range, 17–88 years)
were identified in which both pathology reports
and ultrasound images were available. From the
alphabetized list generated, the first 500 nodules
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were evaluated immediately by the cytologists to
confirm sample adequacy.
Ultrasound Interpretation
In this retrospective study the ultrasound im­
and 3, carcinoma. Type 1 nodules were determined
to be nodules that did not require biopsy; types 2
and 3 were nodules requiring biopsy.
Data Analysis

were reviewed. This HIPAA-compliant study was
approved by our institutional review board with
a waiver of informed consent. We analyzed the
accuracy of individual sonographic features and
of 10 discrete recognizable morphologic patterns
in the prediction of benign histologic findings.
Ultrasound Technique
All diagnostic ultrasound examinations and
FNA biopsies were performed with an Acuson
×300 or Antares unit (both Siemens Healthcare).
All FNA biopsies were performed by a group of
four cytologists (average experience, 5 years)
under ultrasound guidance by one of five
radiologists (average experience, 20.5 years). The
biopsies were performed with 25-gauge spinal
needles in most instances; a 27-gauge needle was
used for hypervascular lesions. At least two passes
were made for each nodule (average, 3.2 passes
per nodule; range, 2–6 passes). All specimens
ages of all nodules were reviewed in consensus by
two blinded radiologists: one an attending radi­
ologist with 31 years of ultrasound experience, the
other a second-year radiology resident. Each
nodule was evaluated for the presence or absence
of individual sonographic features and was as­
signed one of 10 distinct recognizable mor­pho­
logic patterns.
Histologic Analysis
The final diagnosis was based on the cytologic
result; final pathologic confirmation was limited
to the 20 malignant tumors resected. In the
20 patients with these tumors, there was no
discrepancy between the initial cytologic and the
final pathologic result. The cytologic results were
divided into three categories: 1, benign nodules,
including colloid nodules, hyperplastic nodules,
and localized thyroiditis; 2, intermediate nodules,
including follicular and Hürthle cell neoplasms;
The sensitivity, specificity, positive predictive
value, and negative predictive value were defined
for each individual sonographic feature in the
detection of nonbenign masses. The Blyth-Still-
Casella procedure for construction of exact CI for
a binomial proportion was used to derive a 95% CI
for the negative predictive value associated with
each classification factor when used to identify
benign masses. All reported p values were two-
sided significance levels and were declared
statistically significant at less than 0.05. SAS
software (version 9.0, SAS Institute) was used
for all statistical computations. Each p value was
derived from a Fisher’s exact test performed to
determine whether the classification factor was
associated with benignity.
Results
The individual ultrasound features of each
nodule analyzed were size, number, texture

A B C

Fig. 1—Individual ultrasound features of nodules.

A, 85-year-old woman with subcentimeter papillary
carcinoma. Ultrasound scan shows hypoechoic
nodule.
B, 46-year-old woman with papillary carcinoma.
Ultrasound scan shows nodule with ill-defined
borders.
C, 36-year-old man with papillary carcinoma.
Ultrasound scan shows microcalcifications
(arrow), which are easily confused with comet-tail
shadowing. Important finding is hypoechogenicity of
nodule.
D, 37-year-old woman with medullary carcinoma.
Ultrasound scan shows macrocalcification.
E, 37-year-old woman with papillary carcinoma.
Color Doppler ultrasound image shows hypervascular
nodule.
D E

208 AJR:193, July 2009

 Thyroid Ultrasound

TABLE 1:  Diagnostic Characteristics of Each Classification in Identification of Benign Masses

Positive Predictive Negative Predictive
Classification Sensitivity (%) Specificity (%) Value (%) Value (%) p
Presence of sharp border 62.5 (25/40) 61.7 (284/460) 12.4 (25/201) 95.0 (284/299) 0.0017
Absence of calcification 25.0 (10/40) 93.3 (429/460) 24.4 (10/41) 93.5 (429/459) 0.0005
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Absence of halo 32.5 (13/40) 75.9 (349/460) 10.5 (13/124) 92.8 (349/376) 0.0731
Presence of hyperechogenicity 100.0 (40/40) 8.9 (41/460) 8.7 (40/459) 100.0 (41/41) 0.0282
Absence of hypoechogenicity 52.5 (21/40) 92.2 (424/460) 36.8 (21/57) 95.7 (424/443) < 0.0001
Absence of isoechogenicity 35.0 (14/40) 78.7 (362/460) 12.5 (14/112) 93.3 (362/388) 0.023
Absence of hypervascularity 35.0 (14/40) 90.4 (416/460) 24.1 (14/58) 94.1 (416/442) < 0.0001
Presence of spongiform configuration 90.0 (36/40) 57.8 (266/460) 15.7 (36/230) 98.5 (266/270) < 0.0001
Absence of edge refraction 7.5 (3/40) 97.8 (450/460) 23.1 (3/13) 92.4 (450/487) 0.0625
Absence of ring vascularity 22.5 (9/40) 92.2 (424/460) 20.0 (9/45) 93.2 (424/455) 0.0042
Presence of classification 1–4 100.0 (40/40) 65.9 (303/460) 20.3 (40/197) 100.0 (303/303) < 0.0001
Note—Values in parentheses are numbers of nodules.

(Fig. 1A), margination (Fig. 1B), presence of
internal densities or calcifications (Figs. 1C
and 1D), edge refraction, and vascularity rel-
ative to the rest of the gland [13, 25, 26] (Fig.
1E). Analysis of the presence or absence of
individual sonographic features revealed no
feature with consistently high sensitivity or
specificity for malignancy (Table 1). In our
study, sensitivity for the presence or absence
of specific features was 35–100% and spec-
ificity, 8.9–97.8%. There was no correlation
between diagnosis and nodule size, which
was categorized as less than 1 cm (n = 7), 1–2
cm (n = 288), and larger than 2 cm (n = 206)
(Table 2). However, several features were
found to have a statistically significant neg-
ative predictive value. These individual fea-
tures, the absence of which was common in
benign disease, included calcification, halo,
hypoechogenicity, isoechogenicity, and ring
or peripheral hypervascularity.
Each nodule was assigned to one of 10 dis-
crete morphologic groupings. These patterns,
which were based on a previous report [23]
and expanded according to our experience,
were as follows: 1, spongiform without hy-
pervascularity (Fig. 2A); 2, cyst with avascu-
lar colloid plug (Fig. 2B); 3, giraffe pattern
(Fig. 2C) with blocks of hyperechogenicity,
or white, separated by bands of hypoechoge-
nicity, or black; 4, uniform hyperechogenici-
ty (“white knight”) (Fig. 2D); 5, intense hy-
pervascularity (“red light”) (Fig. 2E); 6,
hypoechogenicity (Fig. 2F); 7, isoechogenic-
ity without halo (Fig. 2G); 8, isoechogenicity
with halo (Fig. 2H); 9, “ring of fire,” or nod-
ules with intense peripheral vascularity (Fig.
2I); and 10, other (Fig. 2J), or a mixed pattern
or pattern that did not fit the other categories
TABLE 2:  Size Versus Diagnosis
Nodule Diameter (cm)
Diagnosis <1 1–2 >2
Benign 6 265 190
Follicular 0 10 10
Malignant 1 13 6
Total 7 288 206
Note—There was no correlation between diagnosis and nodule size.
(Table 3). A distinct pattern emerged in which has replaced blind surgical excision as the
it became evident that there were specific procedure of choice in the diagnosis of thy-
morphologic groupings or patterns that were roid nodules. Use of FNA has led to a con-
accurate predictors of benign disease. Specif- siderable decrease in the number of surgical
ically, there were no malignant nodules in the excisions and to a twofold increase in the di-
303 patients (61%) with patterns 1–4 (Table agnosis of carcinoma [4, 5, 29]. The relative
4). Spongiform nonhypervascular masses ease of FNA compared with surgery and the
were the most common type of nodule seen, increased frequency and refinement of imag-
210 of 210 being found benign at FNA biop- ing studies has resulted in what some authors
sy. All 53 of the cysts with internal colloid have referred to as an epidemic of thyroid
clot, all 23 giraffe pattern nodules, and all 17 nodules [3, 30].
hyperechoic nodules were benign. The re- In view of their ubiquity, it is not feasible to
sults in patterns 5–10 were unpredictable, biopsy every thyroid nodule discovered with
ranging from 35 of 37 isoechoic nodules ultrasound. Reasons for limiting thyroid bi-
without halo biopsied being benign to only opsy, which is relatively painless and safe, in-
31 of 45 hypoechoic nodules being benign. clude the small percentage of malignant le-
sions, the small number of cases of thyroid
Discussion cancer in which early diagnosis may actually
A thyroid nodule is a discrete lesion, have an influence, the economic and societal
sonographically distinct from the surround- costs, the strain on radiology resources, and
ing thyroid parenchyma [27]. Rather than a the patient uncertainty and anxiety incumbent
single disease, nodules are manifestations of on a potentially malignant diagnosis. Hence,
a gamut of thyroid diseases [28]. Although reliable guidelines for nodules that may not
some thyroid nodules may be discovered at require biopsy have become essential.
physical examination, many are incidental Not surprisingly in view of the experi-
findings of other imaging studies, such as ence of other authors [31], we concluded that
CT and MRI of the neck or chest and carotid no individual sonographic feature had both
ultrasound imaging. FNA of thyroid nodules high sensitivity and high specificity in the

AJR:193, July 2009 209

 Bonavita et al.
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A B C

D E F

G H I
Fig. 2—Morphologic patterns.
A, 41-year-old man with colloid nodule. Ultrasound scan shows spongiform nodule. Similarity of nodule to
water-filled sponge is evident.
B, 52-year-old man with colloid cyst. Ultrasound scan shows cyst with colloid clot. When cystic portion of
nodule is subtracted, type 1 or spongiform nodules remain.
C, 21-year-old woman with Hashimoto’s thyroiditis. Ultrasound scan shows nodule that looks like giraffe hide,
having light blocks separated by black bands.
D, 34-year-old woman with Hashimoto’s thyroiditis. Ultrasound scan shows “white knight,” or hyperechoic,
nodule.
E, 61-year-old woman with follicular adenoma. Color Doppler ultrasound image shows “red light,” or
hypervascular, nodule.
F, 29-year-old woman with papillary carcinoma. Ultrasound scan shows hypoechoic nodule.
G, 70-year-old woman with papillary carcinoma. Ultrasound scan shows isoechoic nodule without halo.
Coincidental microcalcifications (arrows) are evident.
H, 25-year-old man with nodular goiter. Ultrasound scan shows isoechoic nodule with halo.
J I, 55-year-old woman with hyperplastic nodule. Color Doppler ultrasound image shows “ring of fire,” or
peripheral hypervascularity.
J, 61-year-old man with colloid nodule. Ultrasound scan shows nodule that fits into no other pattern.

210 AJR:193, July 2009

 Thyroid Ultrasound

TABLE 3:  Features of Morphologic Types of Thyroid Nodules

Pattern Texture Vascularity Margins Densities
1, Spongiform or “puff pastry” Spongiform internal cysts None or isovascular Well-defined Present or absent comet tail
2, Cyst with colloid clot Cystic with mural clot None or isovascular Well-defined Present or absent comet tail
3, Giraffe Hyperechoic block, black bands None or isovascular Any Absent
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4, Hyperechoic, or “white knight” Hyperechoic None or isovascular Well-defined Absent

5, Intensely hypervascular, or “red light” Any Central hypervascularity Any Present or absent
6, Hypoechoic Hypoechoic None or isovascular Any Present or absent
7, Isoechoic without halo Isoechoic None or isovascular Any Present or absent
8, Isoechoic with halo Isoechoic None or isovascular Well-defined Present or absent
9, “Ring of fire” Any Peripheral hypervascularity Well-defined Present or absent
10, Other Any Any Any Present or absent

TABLE 4:  Number of Nodules With Pattern Categorized by Suggested Management and Diagnosis (n = 500)
Benign, Watch (n = 460) Malignant, Biopsy (n = 40)
Pattern Total Colloid Hashimoto’s Thyroiditis Hyperplasia Total Follicular Malignant
1, Spongiform 210 196 6 8 0 0 0
2, Cyst with colloid clot 53 52 1 0 0 0 0
3, Giraffe 23 12 10 1 0 0 0
4, “White knight” 17 9 8 0 0 0 0
5, “Red light” 37 29 5 3 15 11 4
6, Hypoechoic 31 19 8 4 14 1 13
7, Isoechoic without halo 35 26 4 5 2 0 2
8, Isoechoic with halo 37 33 1 3 4 1 3
9, “Ring of fire” 6 5 0 1 4 4 0
10, Other 11 10 1 0 1 0 1
Note—Patterns 1–4 are invariably associated with benign conditions. Patterns 5–10 are variable.

detection of malignancy. Nonetheless, many
of these previously described high-risk fea-
tures, such as calcification, hypoechogenic-
ity, poor definition, and hypervascularity,
were found to be absent over and over again
in nodules that did not require biopsy.
The persistent combination of some of
these common individual ultrasound charac-
teristics, or, more properly, their absence, led
us to consider a more pattern-oriented ap-
proach, such as that advocated by Reading
et al. [23] as an alternative to the analysis of
individual features. Those authors described
eight typical appearances of commonly en-
countered benign and malignant nodules, al-
lowing them to separate more than one half
of thyroid nodules into those that could be
observed versus those requiring biopsy. Ac-
cording to their results, the following four
classic patterns necessitate biopsy: 1, a hy-
poechoic nodule with microcalcifications;
2, coarse calcifications in a hypoechoic nod-
ule; 3, well-marginated, ovoid, solid nodules
with a thin hypoechoic halo; and 4, a sol-
id mass with refractive shadowing from the
edges, which is believed to occur as a result
of fibrosis. The four classic patterns of nod-
ules that did not require biopsy in that series
were the following: 1, small (< 1 cm) colloid-
filled cystic nodules; 2, a nodule with a hon-
eycomb appearance consisting of internal
cystic spaces with thin echogenic walls; 3,
a large predominantly cystic nodule; and 4,
diffuse multiple small hypoechoic nodules
with intervening echogenic bands, which are
indicative of Hashimoto’s thyroiditis.
Like Reading et al. [23], we found that
use of a pattern approach to thyroid nod-
ules is highly sensitive and specific for the
presence of benignity. Our patterns differed
somewhat from those proposed previously,
yet there are definite similarities. Analysis
of our data revealed four patterns that were
invariably benign at FNA biopsy (Table 5).
The most common overall pattern is a nodule
with diffuse internal linear cysts, described
as spongiform or honeycomb, our type 1 pat-
tern. In our cases, this finding was common-
ly described as a “puff pastry” pattern simi-
lar to the ultrathin layers of flaky pastry in
desserts such as napoleons. This pattern was
characteristic of colloid nodules or goiter.
The only spongiform nodule not classically
benign was a single nodule that also was in-
tensely hypervascular. Our type 1 or spongi-
form nodule consequently is defined as avas-
cular or, occasionally, isovascular in relation
to the rest of the gland.
The second pattern (type 2) was a cystic
nodule containing a central plug of avascular
colloid, similar to the previously described
small or large cyst patterns [23]. In our initial
analysis of individual features, size of cyst
was deemed insignificant. Important, howev-
er, was the characterization of the plug as
avascular and puff pastry. All of these nodules

AJR:193, July 2009 211

 Bonavita et al.

TABLE 5:  Patterns of Nodules That Do Not Require Biopsy Versus Patterns of Reading et al. [23]
Current Study Classification of Reading et al.
1, Spongiform, or “puff pastry” 2, Honeycomb of internal cystic spaces with thin echogenic walls
2, Cyst with colloid clot 1, Small (< 1 cm) colloid-filled cystic nodules; 3, large predominantly cystic nodule
3, Giraffe 4, Diffuse, multiple small hypoechoic nodules with intervening echogenic bands indicative of Hashimoto’s thyroiditis
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4, Hyperechoic, or “white knight”

TABLE 6:  Patterns of Nodules Requiring Biopsy Versus Patterns of Reading et al. [23]
Current Study: Indeterminate Finding, Biopsy Necessary Reading et al.: High Risk of Malignancy, Biopsy Necessary
5, “Red light,” central hypervascularity
6, Hypoechoic 1, Hypoechoic nodule with microcalcifications; 2, coarse calcifications in a hypoechoic nodule
7, Isoechoic without halo 4, Solid mass with refractive shadowing from the edges, believed to be due to fibrosis
8, Isoechoic with halo 3, Well-marginated, ovoid, solid nodule with a thin hypoechoic halo
9, “Ring of fire,” peripheral vascularity
10, Other

were also colloid nodules. If the cystic portion
of the lesion is subtracted visually, a type 1
spongiform nodule remains. The third pattern
(type 3), or giraffe pattern, was characterized
by globular areas of hyperechogenicity sur-
rounded by linear thin areas of hypoechoge-
nicity, similar to the two-tone blocklike color-
ing of a giraffe. This pattern was quite
characteristic of Hashimoto’s thyroiditis. A
variation of this pattern is our type 4 “white
knight,” or hyperechoic, nodule, which was
found commonly to be a regenerative nodule
of Hashimoto’s thyroiditis.
Analysis of our other patterns revealed
more variability in final cytologic findings
(Table 6). Such nodules included both in-
significant and significant lesions with such
variability that prediction before biopsy was
not reliable. These nodules had the four biop-
sy-recommendation patterns described earli-
er, such as isoechoic nodule with a surround-
ing halo or refractive edges, which came to be
simplified in our series as isoechoic nodules
with or without a halo (types 7 and 8). A hy-
poechoic nodule with or without central mi-
crocalcification or with central macrocalcifi-
cation in other series [25, 26, 32], for which
biopsy was recommended, was the most wor-
risome pattern (type 6) in our study.
We identified other common patterns, in-
cluding the type 5 “red light” pattern, or an
intensely hypervascular lesion that on Dop-
pler images glowed like a red stoplight. This
pattern was commonly seen in lesions with
abundant cellularity, including, commonly,
follicular neoplasms and, less commonly,
hyperplastic nodules and carcinoma. Other
nodule types included type 9 ring-of-fire nod-
ules with intense peripheral vascularity and
nodules described as other (type 10), which
did not fit any of the classic patterns. Calci-
fication, although commonly seen in nodules
requiring biopsy, was never seen as an iso-
lated finding. The likelihood of benignity of
these nodules (type 5–10) ranged from 60%
(type 9, ring of fire) to 91% (type 10, other).
Because of this lack of predictability, we be-
lieved that these nodules should be consid-
ered for FNA biopsy.
The limitations of our study are related to
the fact that most of the diagnoses were based
on cytologic rather than histologic findings,
the retrospective nature of the study, and the
fact that nodule characterization was depen-
dent on only two observers. The readers were
blinded to the cytologic results at the time of
nodule characterization. The period 2005–
2007 was chosen to minimize the potential
for recall bias. To answer our concerns with
respect to these limitations, we are preparing
a study in which we train radiologists with
varying degrees of experience in this pattern
approach. A series of consecutive thyroid bi-
opsies will be chosen prospectively in the
weeks before their performance, and the im-
ages will be shown to these readers, who will
decide whether biopsy should be performed.
Analysis of interobserver variability for as-
signing nodules to a specific pattern will be
analyzed, as will the characterizations with
final cytologic result.
We conclude that biopsy of a large number
of thyroid nodules (in our study, 61%) can be
avoided when a pattern approach to nodule
characterization is used. Specific morpho-
logic patterns are highly predictive of benig-
nity. Specifically, a nodule that has a uniform
nonhypervascular spongiform appearance,
is a cystic lesion with a colloid clot, has a gi-
raffelike pattern, or is diffusely hyperechoic
can be observed rather than biopsied. If, con-
versely, a nodule does not correspond to one
of these four patterns, according to our data
biopsy should be performed regardless of the
individual features or pattern of the nodule.
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