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AJR:193, July 2009 207

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 evaluatethe 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

Pattern Recognition of Benign

Nodules at Ultrasound of theThyroid: Which Nodules CanBe Left Alone?

John A. Bonavita1

Jason Mayo1

James Babb1

Genevieve Bennett1

Thaira Oweity2

Michael Macari1

Joseph Yee1

Bonavita JA, Mayo J, Babb J, et al.

1

Department of Radiology, Langone Medical Center, NewYork University School of Medicine, 550 First Ave., New

York, NY 10016. Address correspondence to J. Bonavita

([email protected]).

2Department of Pathology, Langone Medical Center, New

York University School of Medicine, New York, NY.

Neuroradiology/Head and Neck Imaging • Original Research

AJR 2009; 193:207–213

0361–803X/09/1931–207

© American Roentgen Ray Society

One 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-

ing a rapid transition from nuclear medicineto 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,

Keywords: fine-needle aspiration, nodule, thyroid,

ultrasound

DOI:10.2214/AJR.08.1820

Received September 12, 2008 ; accepted after revision

October 24, 200 8.

OBJECTIVE. The purpose of this study was to evaluate morphologic features predictive

of benign thyroid nodules.

MATERIALS AND METHODS. From a registry of the records of 1,232 fine-needle

aspiration biopsies performed jointly by the cytology and radiology departments at a single

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-

ated, the first 500 nodules were reviewed. We analyzed the accuracy of individual sonograph-ic features and of 10 discrete recognizable morphologic patterns in the prediction of benign

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.

Bonavita et al.Thyroid Ultrasound

Neuroradiology/Head and Neck ImagingOriginal Research





AJR:193, July 2009 209

Thyroid Ultrasound

(Fig. 1A), margination (Fig. 1B), presence of

internal densities or calcifications (Figs. 1Cand 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 hypervascular ity.

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 3). A distinct pattern emerged in which

it became evident that there were specific

morphologic groupings or patterns that were

accurate predictors of benign disease. Specif-

ically, there were no malignant nodules in the

303 patients (61%) with patterns 1–4 (Table

4). Spongiform nonhypervascular masses

were the most common type of nodule seen,

210 of 210 being found benign at FNA biop-

sy. All 53 of the cysts with internal colloid

clot, all 23 giraffe pattern nodules, and all 17

hyperechoic nodules were benign. The re-

sults in patterns 5–10 were unpredictable,

ranging from 35 of 37 isoechoic nodules

without halo biopsied being benign to only

31 of 45 hypoechoic nodules being benign.

DiscussionA thyroid nodule is a discrete lesion,

sonographically distinct from the surround-

ing thyroid parenchyma [27]. Rather than a

single disease, nodules are manifestations of

a gamut of thyroid diseases [28]. Although

some thyroid nodules may be discovered at

physical examination, many are incidental

findings of other imaging studies, such as

CT and MRI of the neck or chest and carotid

ultrasound imaging. FNA of thyroid nodules

has replaced blind surgical excision as the

procedure of choice in the diagnosis of thy-

roid nodules. Use of FNA has led to a con-

siderable decrease in the number of surgical

excisions and to a twofold increase in the di-

agnosis of carcinoma [4, 5, 29]. The relative

ease of FNA compared with surgery and the

increased frequency and refinement of imag-

ing studies has resulted in what some authors

have referred to as an epidemic of thyroid

nodules [3, 30].

In view of their ubiquity, it is not feasible to

biopsy every thyroid nodule discovered with

ultrasound. Reasons for limiting thyroid bi-

opsy, which is relatively painless and safe, in-

clude the small percentage of malignant le-

sions, the small number of cases of thyroid

cancer in which early diagnosis may actuallyhave an influence, the economic and societal

costs, the strain on radiology resources, and

the patient uncertainty and anxiety incumbent

on a potentially malignant diagnosis. Hence,

reliable guidelines for nodules that may not

require biopsy have become essential.

Not surprisingly in view of the experi-

ence of other authors [31], we concluded that

no individual sonographic feature had both

high sensitivity and high specificity in the

TABLE 1: Diagnostic Characteristics of Each Classif ication in Identification of Benign Masses

Classification Sensitivity (%) Specificity (%)Positive Predictive

Value (%)Negative Predictive

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

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.

TABLE 2: Size Versus Diagnosis

Diagnosis

Nodule Diameter (cm)

< 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 bet ween diagnosis and nodule size.



210 AJR:193, July 2009

Bonavita et al.

A

Fig. 2—Morphologic patterns.A, 41-year-old man with colloid nodule. Ultrasound scan shows spongiform nodule. Similarity of nodule towater-filled sponge is evident.B, 52-year-old man with colloid cyst. Ultrasound scan shows cyst with colloid clot. When cystic portion ofnodule 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 ult rasound 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.I, 55-year-old woman with hyperplastic nodule. Color Doppler ultrasound image shows “ring of fire,” orperipheral hypervascularity.J, 61-year-old man with colloid nodule. Ultrasound scan shows nodule that fits into no other pattern.

CB

D FE

G IH

J



AJR:19 3, July 200 9 211

Thyroid Ultrasound

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 describedeight 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 areindicative 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 relationto 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

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

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)

Pattern

Benign, Watch (n = 460) Malignant, Biopsy (n = 40)

Total Colloid Hashimoto’s Thyroiditis Hyperplasia Total Follicular Malignant

1, Spongiform 210 196 6 8 0 0 02, 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—Pat terns 1–4 are invariably associated with benign conditions. Patterns 5–10 are variable.



212 AJR:193, July 2009

Bonavita et al.

were also colloid nodules. If the cystic portionof 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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