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 evaluate the accuracy of such a morphologic feature–oriented approach to the identification of be-nign thyroid nodules.

Materials and MethodsPatients

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 the Thyroid: Which Nodules Can Be 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.

1Department 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).

2Department of Pathology, Langone Medical Center, New York University School of Medicine, New York, NY.

Neuroradiolog y / Head and Neck Imaging • Or ig ina l 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 medicine 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,

Keywords: fine-needle aspiration, nodule, thyroid, ultrasound

DOI:10.2214/AJR.08.1820

Received September 12, 2008; accepted after revision October 24, 2008.

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

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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 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 TechniqueAll 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

were evaluated immediately by the cytologists to confirm sample adequacy.

Ultrasound InterpretationIn this retrospective study the ultrasound im-

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 mor pho-logic patterns.

Histologic AnalysisThe 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;

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 AnalysisThe 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.

ResultsThe individual ultrasound features of each

nodule analyzed were size, number, texture

D E

A CB

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.

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(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 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 actually have 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 Classification 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 between diagnosis and nodule size.

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A

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.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.

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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

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 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.

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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.

References 1. Ezzat S, Sarti DA, Cain DR, et al. Thyroid inciden-

talomas: prevalence by palpation and ultrasonog-

raphy. Arch Intern Med 1994; 154:1838–1840

2. Frates MC, Benson CB, Charboneau JW, et al.

Management of thyroid nodules detected at US:

Society of Radiologists in Ultrasound consensus

conference statement. Radiology 2005; 237:794–

800

3. Brander AE, Viikinkoski VP, Nickels JI, Kivisaari

LM. Importance of thyroid abnormalities detect-

ed at US screening: a 5-year follow-up. Radiology

2000; 215:801–806

4. Jemal A, Murray T, Ward E, et al. Cancer statis-

tics, 2005. CA Cancer J Clin 2005; 55:10–30 [Er-

ratum in CA Cancer J Clin 2005; 55:259]

5. Harnsberger H. Diagnostic imaging: head and

neck. Salt Lake City, UT: Amirsys, 2004:24–40

6. Kountakis SE, Skoulas IG, Maillard AA. The ra-

diologic work-up in thyroid surgery: fine-needle

biopsy versus scintigraphy and ultrasound. Ear

Nose Throat J 2002; 81:151–154

7. Rago T, Vitti P, Chiovato L, et al. Role of conven-

tional ultrasonography and color flow-Doppler

sonography in predicting malignancy in “cold”

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

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

4, Hyperechoic, or “white knight”

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ww

w.a

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line.

org

by 3

9.21

9.91

.180

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04/2

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dres

s 39

.219

.91.

180.

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yrig

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RR

S. F

or p

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se o

nly;

all

righ

ts r

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AJR:193, July 2009 213

Thyroid Ultrasound

thyroid nodules. Eur J Endocrinol 1998; 138:41–46

8. Giuffrida D, Gharib H. Controversies in the man-

agement of cold, hot, and occult thyroid nodules.

Am J Med 1995; 99:642–650

9. Papini E, Guglielmi R, Bianchini A, et al. Risk of

malignancy in nonpalpable thyroid nodules: pre-

dictive value of ultrasound and color-Doppler fea-

tures. J Clin Endocrinol Metab 2002; 87:1941–

1946

10. Jun P, Chow LC, Jeffrey RB. The sonographic

features of papillary thyroid carcinomas: pictorial

essay. Ultrasound Q 2005; 21:39–45

11. Kim EK, Park CS, Chung WY, et al. New sono-

graphic criteria for recommending fine-needle

aspiration biopsy of nonpalpable solid nodules of

the thyroid. AJR 2002; 178:687–691

12. Koike E, Noguchi S, Yamashita H, et al. Ultra-

sonographic characteristics of thyroid nodules:

prediction of malignancy. Arch Surg 2001; 136:

334–337

13. Chan BK, Desser TS, McDougall IR, et al. Com-

mon and uncommon sonographic features of pap-

illary thyroid carcinoma. J Ultrasound Med 2003;

22:1083–1090

14. Ahuja A, Chick W, King W, Metreweli C. Clinical

significance of the comet-tail artifact in thyroid

ultrasound. J Clin Ultrasound 1996; 24:129–133

15. Kovacevic DO, Skurla MS. Sonographic diagno-

sis of thyroid nodules: correlation with the results

of sonographically guided fine-needle aspiration

biopsy. J Clin Ultrasound 2007; 35:63–67

16. Frates MC, Benson CB, Doubilet PM, et al. Preva-

lence and distribution of carcinoma in patients

with solitary and multiple thyroid nodules on

sonography. J Clin Endocrinol Metab 2006; 91:

3411–3417

17. Cooper DS, Doherty GM, Haugen BR, et al. Man-

agement guidelines for patients with thyroid nod-

ules and differentiated thyroid cancer. Thyroid

2006; 16:109–142

18. Pacini F, Schlumberger M, Dralle H, Elisei R,

Smit JW, Wiersinga W; European Thyroid Cancer

Taskforce. European consensus for the manage-

ment of patients with differentiated thyroid carci-

noma of the follicular epithelium. Eur J Endo-

crinol 2006; 154:787–803

19. British Thyroid Association and Royal College of

Physicians. Guidelines for the management of thy-

roid cancer in adults. London, UK: Publication

Unit of the Royal College of Physicians, 2002

20. Rodrigues FJ, Limbert ES, Marques AP, et al.;

Grupo de Estudo da Tiróide. Treatment and fol-

low up protocol in differentiated thyroid carcino-

mas of follicular origin [in Portuguese]. Acta Med

Port 2005; 18:2–16

21. Società Italiana di Endocrinologia, Associazione

Italiana di Medicina Nucleare ed Imaging Mole-

colare, Associazione Italiana di Fisica Medica.

Linee Guida SIE-AIMN-AIFM per il trattamento

e follow-up del carcinoma tiroideo differenziato

della tiroide. Rome, Milan, and Gazzada, Italy:

SIE, AIMN, and AIFM, 2004:1–75

22. Van De Velde CJ, Hamming JF, Goslings BM, et

al. Report of the consensus development confer-

ence on the management of differentiated thyroid

cancer in The Netherlands. Eur J Cancer Clin On-

col 1988; 24:287–292

23. Reading CC, Charboneau JW, Hay ID, Sebo TJ.

Sonography of thyroid nodules: a “classic pattern”

diagnostic approach. Ultrasound Q 2005; 21:157–

165

24. Hegedus L. Thyroid ultrasound. Endocrinol Me-

tab Clin North Am 2001; 30:339–360

25. Hoang JK, Lee WK, Lee M, Johnson D, Farrell S.

US features of thyroid malignancy: pearls and pit-

falls. RadioGraphics 2007; 27:847–860

26. Takashima S, Fukuda H, Nomura N, Kishimoto

H, Kim T, Kobayashi T. Thyroid nodules: reevalu-

ation with ultrasound. J Clin Ultrasound 1995;

23:179–184

27. Vandermeer FQ, Wong-You-Cheong J. Thyroid nod-

ules: when to biopsy. Appl Radiol 2007; 36:8–19

28. Pacini F, Burroni L, Ciuoli C, Di Cairano G, Gua-

rino E. Management of thyroid nodules: a clinico-

pathological, evidence-based approach. Eur J

Nucl Med Mol Imaging 2004; 31:1443–1449

29. Castro MR, Gharib H. Thyroid fine-needle aspi-

ration biopsy: progress, practice, and pitfalls. En-

docr Pract 2003; 9:128–136

30. Ross DS. Nonpalpable thyroid nodules: managing

an epidemic. J Clin Endocrinol Metab 2002; 87:

1938–1940

31. Sahin M, Sengul A, Berki Z, Tutuncu NB, Gu-

vener ND. Ultrasound-guided fine-needle aspira-

tion biopsy and ultrasonographic features of in-

fracentimetric nodules in patients with nodular

goiter: correlation with pathological findings. En-

docr Pathol 2006; 17:67–74

32. Iannuccilli JD, Cronan JJ, Monchik JM. Risk for

malignancy of thyroid nodules as assessed by

sonographic criteria: the need for biopsy. J Ultra-

sound Med 2004; 23:1455–1464

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