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Neuroradiolog y / Head and Neck Imaging Original Research

Bonavita et al. Thyroid Ultrasound Neuroradiology/Head and Neck Imaging Original Research

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Pattern Recognition of Benign Nodules at Ultrasound of the Thyroid: Which Nodules Can Be Left Alone?
John A. Bonavita1 Jason Mayo1 James Babb1 Genevieve Bennett 1 Thaira Oweity 2 Michael Macari1 Joseph Yee1
Bonavita JA, Mayo J, Babb J, et al.

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 ne-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 identied for whom both a pathology report and ultrasound images were available. From the alphabetized list generated, the rst 500 nodules were reviewed. We analyzed the accuracy of individual sonographic features and of 10 discrete recognizable morphologic patterns in the prediction of benign histologic ndings. RESULTS. We found that grouping of thyroid nodules into reproducible patterns of morphology, or pattern recognition, rather than analysis of individual sonographic features, was extremely accurate in the identication of benign nodules. Four specic patterns were identied: spongiform conguration, cyst with colloid clot, giraffe pattern, and diffuse hyperechogenicity, which had a 100% specicity for benignity. In our series, identication of nodules with one of these four patterns could have obviated more than 60% of thyroid biopsies. CONCLUSION. Recognition of specic morphologic patterns is an accurate method of identifying benign thyroid nodules that do not require cytologic evaluation. Use of this approach may substantially decrease the number of unnecessary biopsy procedures. ne of the consequences of increased use of imaging has been the discovery of incidentalomas, or pseudodiseases, that are common in the general population but have no or minor clinical signicance. Once such incidentaloma, 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 incidence of malignancy is quite low, 37% [35]. In the late 1990s, articles began to appear questioning the reliability of radiotracer uptake as a predictor of benignity, occasioning a rapid transition from nuclear medicine to ultrasound for evaluation of the thyroid [68]. 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 between specic sonographic features of thyroid nodules and malignancy [2, 1016]. Although guidelines have been established,

Keywords: ne-needle aspiration, nodule, thyroid, ultrasound DOI:10.2214/AJR.08.1820 Received September 12, 2008; accepted after revision October 24, 2008.
1 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.

such as those of the Society of Radiologists in Ultrasound, the American Thyroid Association, and the European Thyroid Association [2, 1722], 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 specicity and sensitivity of specic ultrasound features in the prediction of malignancy. Some authors [23, 24] advocate a changed approach of recognition of specic patterns rather than individual ultrasound features in separation of nodules 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 identication of benign thyroid nodules. Materials and Methods Patients
Among the records of 1,232 ne-needle aspir ation (FNA) biopsies performed jointly by the cytology and radiology departments at a single institution from January 2005 to December

AJR 2009; 193:207213 0361803X/09/1931207 American Roentgen Ray Society

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2007, the cases of 650 patients (436 women, 64 men; average age, 54.7 years; range, 1788 years) were identied in which both pathology reports and ultrasound images were available. From the alphabetized list generated, the rst 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 ndings. were evaluated immediately by the cytologists to conrm sample adequacy. and 3, carcinoma. Type 1 nodules were determined to be nodules that did not require biopsy; types 2 and 3 were nodules requiring biopsy.

Ultrasound Interpretation
In 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.

Data Analysis
The sensitivity, specicity, positive predictive value, and negative predictive value were dened for each individual sonographic feature in the detection of nonbenign masses. The Blyth-StillCasella 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 classication factor when used to identify benign masses. All reported p values were twosided signicance levels and were declared statistically signicant 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 Fishers exact test performed to determine whether the classication factor was associated with benignity.

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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 ve 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, 26 passes). All specimens

Histologic Analysis
The nal diagnosis was based on the cytologic result; nal pathologic conrmation 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 nal 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 Hrthle cell neoplasms;

Results The individual ultrasound features of each nodule analyzed were size, number, texture

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-dened borders. C, 36-year-old man with papillary carcinoma. Ultrasound scan shows microcalcications (arrow ), which are easily confused with comet-tail shadowing. Important nding is hypoechogenicity of nodule. D, 37-year-old woman with medullary carcinoma. Ultrasound scan shows macrocalcication. E, 37-year-old woman with papillary carcinoma. Color Doppler ultrasound image shows hypervascular nodule.

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Thyroid Ultrasound TABLE 1: Diagnostic Characteristics of Each Classification in Identification of Benign Masses
Classication Presence of sharp border Absence of calcication Downloaded from www.ajronline.org by 39.219.91.180 on 04/21/13 from IP address 39.219.91.180. Copyright ARRS. For personal use only; all rights reserved Absence of halo Presence of hyperechogenicity Absence of hypoechogenicity Absence of isoechogenicity Absence of hypervascularity Absence of edge refraction Absence of ring vascularity Presence of classication 14 Sensitivity (%) 62.5 (25/40) 25.0 (10/40) 32.5 (13/40) 100.0 (40/40) 52.5 (21/40) 35.0 (14/40) 35.0 (14/40) 90.0 (36/40) 7.5 (3/40) 22.5 (9/40) 100.0 (40/40) Specicity (%) 61.7 (284/460) 93.3 (429/460) 75.9 (349/460) 8.9 (41/460) 92.2 (424/460) 78.7 (362/460) 90.4 (416/460) 57.8 (266/460) 97.8 (450/460) 92.2 (424/460) 65.9 (303/460) Positive Predictive Value (%) 12.4 (25/201) 24.4 (10/41) 10.5 (13/124) 8.7 (40/459) 36.8 (21/57) 12.5 (14/112) 24.1 (14/58) 15.7 (36/230) 23.1 (3/13) 20.0 (9/45) 20.3 (40/197) Negative Predictive Value (%) 95.0 (284/299) 93.5 (429/459) 92.8 (349/376) 100.0 (41/41) 95.7 (424/443) 93.3 (362/388) 94.1 (416/442) 98.5 (266/270) 92.4 (450/487) 93.2 (424/455) 100.0 (303/303) p 0.0017 0.0005 0.0731 0.0282 < 0.0001 0.023 < 0.0001 < 0.0001 0.0625 0.0042 < 0.0001

Presence of spongiform conguration

NoteValues in parentheses are numbers of nodules.

(Fig. 1A), margination (Fig. 1B), presence of internal densities or calcications (Figs. 1C and 1D), edge refraction, and vascularity relative 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 specicity for malignancy (Table 1). In our study, sensitivity for the presence or absence of specic features was 35100% and specicity, 8.997.8%. There was no correlation between diagnosis and nodule size, which was categorized as less than 1 cm (n = 7), 12 cm (n = 288), and larger than 2 cm (n = 206) (Table 2). However, several features were found to have a statistically signicant negative predictive value. These individual features, the absence of which was common in benign disease, included calcication, halo, hypoechogenicity, isoechogenicity, and ring or peripheral hypervascularity. Each nodule was assigned to one of 10 discrete morphologic groupings. These patterns, which were based on a previous report [23] and expanded according to our experience, were as follows: 1, spongiform without hypervascularity (Fig. 2A); 2, cyst with avascular colloid plug (Fig. 2B); 3, giraffe pattern (Fig. 2C) with blocks of hyperechogenicity, or white, separated by bands of hypoechogenicity, or black; 4, uniform hyperechogenicity (white knight) (Fig. 2D); 5, intense hypervascularity (red light) (Fig. 2E); 6, hypoechogenicity (Fig. 2F); 7, isoechogenicity without halo (Fig. 2G); 8, isoechogenicity with halo (Fig. 2H); 9, ring of re, or nodules with intense peripheral vascularity (Fig. 2I); and 10, other (Fig. 2J), or a mixed pattern or pattern that did not t the other categories

TABLE 2: Size Versus Diagnosis


Nodule Diameter (cm) Diagnosis Benign Follicular Malignant Total <1 6 0 1 7 12 265 10 13 288 >2 190 10 6 206

NoteThere was no correlation between diagnosis and nodule size.

(Table 3). A distinct pattern emerged in which it became evident that there were specic morphologic groupings or patterns that were accurate predictors of benign disease. Specifically, there were no malignant nodules in the 303 patients (61%) with patterns 14 (Table 4). Spongiform nonhypervascular masses were the most common type of nodule seen, 210 of 210 being found benign at FNA biopsy. All 53 of the cysts with internal colloid clot, all 23 giraffe pattern nodules, and all 17 hyperechoic nodules were benign. The results in patterns 510 were unpredictable, ranging from 35 of 37 isoechoic nodules without halo biopsied being benign to only 31 of 45 hypoechoic nodules being benign. Discussion A thyroid nodule is a discrete lesion, sonographically distinct from the surrounding 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 ndings 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 thyroid nodules. Use of FNA has led to a considerable decrease in the number of surgical excisions and to a twofold increase in the diagnosis of carcinoma [4, 5, 29]. The relative ease of FNA compared with surgery and the increased frequency and renement of imaging 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 biopsy, which is relatively painless and safe, include the small percentage of malignant lesions, the small number of cases of thyroid cancer in which early diagnosis may actually have an inuence, 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 experience of other authors [31], we concluded that no individual sonographic feature had both high sensitivity and high specicity in the

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H
Fig. 2 Morphologic patterns. A, 41-year-old man with colloid nodule. Ultrasound scan shows spongiform nodule. Similarity of nodule to water-lled 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 Hashimotos thyroiditis. Ultrasound scan shows nodule that looks like giraffe hide, having light blocks separated by black bands. D, 34-year-old woman with Hashimotos 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 microcalcications (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 re, or peripheral hypervascularity. J, 61-year-old man with colloid nodule. Ultrasound scan shows nodule that ts into no other pattern.

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Thyroid Ultrasound TABLE 3: Features of Morphologic Types of Thyroid Nodules


Pattern 1, Spongiform or puff pastry 2, Cyst with colloid clot Downloaded from www.ajronline.org by 39.219.91.180 on 04/21/13 from IP address 39.219.91.180. Copyright ARRS. For personal use only; all rights reserved 3, Giraffe 4, Hyperechoic, or white knight 5, Intensely hypervascular, or red light 6, Hypoechoic 7, Isoechoic without halo 8, Isoechoic with halo 9, Ring of re 10, Other Texture Spongiform internal cysts Cystic with mural clot Hyperechoic block, black bands Hyperechoic Any Hypoechoic Isoechoic Isoechoic Any Any Vascularity None or isovascular None or isovascular None or isovascular None or isovascular Central hypervascularity None or isovascular None or isovascular None or isovascular Peripheral hypervascularity Any Margins Well-dened Well-dened Any Well-dened Any Any Any Well-dened Well-dened Any Densities Present or absent comet tail Present or absent comet tail Absent Absent Present or absent Present or absent Present or absent Present or absent Present or absent Present or absent

TABLE 4: Number of Nodules With Pattern Categorized by Suggested Management and Diagnosis (n = 500)
Benign, Watch (n = 460) Pattern 1, Spongiform 2, Cyst with colloid clot 3, Giraffe 4, White knight 5, Red light 6, Hypoechoic 7, Isoechoic without halo 8, Isoechoic with halo 9, Ring of re 10, Other Total 210 53 23 17 37 31 35 37 6 11 Colloid 196 52 12 9 29 19 26 33 5 10 Hashimotos Thyroiditis 6 1 10 8 5 8 4 1 0 1 Hyperplasia 8 0 1 0 3 4 5 3 1 0 Total 0 0 0 0 15 14 2 4 4 1 Malignant, Biopsy (n = 40) Follicular 0 0 0 0 11 1 0 1 4 0 Malignant 0 0 0 0 4 13 2 3 0 1

NotePatterns 14 are invariably associated with benign conditions. Patterns 510 are variable.

detection of malignancy. Nonetheless, many of these previously described high-risk features, such as calcication, hypoechogenicity, poor denition, 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 characteristics, or, more properly, their absence, led us to consider a more pattern-oriented approach, 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 encountered benign and malignant nodules, allowing them to separate more than one half of thyroid nodules into those that could be observed versus those requiring biopsy. According to their results, the following four classic patterns necessitate biopsy: 1, a hypoechoic nodule with microcalcications; 2, coarse calcications in a hypoechoic nod-

ule; 3, well-marginated, ovoid, solid nodules with a thin hypoechoic halo; and 4, a solid mass with refractive shadowing from the edges, which is believed to occur as a result of brosis. The four classic patterns of nodules that did not require biopsy in that series were the following: 1, small (< 1 cm) colloidlled cystic nodules; 2, a nodule with a honeycomb 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 Hashimotos thyroiditis. Like Reading et al. [23], we found that use of a pattern approach to thyroid nodules is highly sensitive and specic for the presence of benignity. Our patterns differed somewhat from those proposed previously, yet there are denite 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 pattern. In our cases, this nding was commonly described as a puff pastry pattern similar to the ultrathin layers of aky 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 intensely hypervascular. Our type 1 or spongiform nodule consequently is dened as avascular 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 insignicant. Important, however, was the characterization of the plug as avascular and puff pastry. All of these nodules

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Bonavita et al. TABLE 5: Patterns of Nodules That Do Not Require Biopsy Versus Patterns of Reading et al. [23]
Current Study 1, Spongiform, or puff pastry 2, Cyst with colloid clot Downloaded from www.ajronline.org by 39.219.91.180 on 04/21/13 from IP address 39.219.91.180. Copyright ARRS. For personal use only; all rights reserved 3, Giraffe 4, Hyperechoic, or white knight Classication of Reading et al. 2, Honeycomb of internal cystic spaces with thin echogenic walls 1, Small (< 1 cm) colloid-lled cystic nodules; 3, large predominantly cystic nodule 4, Diffuse, multiple small hypoechoic nodules with intervening echogenic bands indicative of Hashimotos thyroiditis

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

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 surrounded by linear thin areas of hypoechogenicity, similar to the two-tone blocklike coloring of a giraffe. This pattern was quite characteristic of Hashimotos 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 Hashimotos thyroiditis. Analysis of our other patterns revealed more variability in nal cytologic ndings (Table 6). Such nodules included both insignicant and signicant lesions with such variability that prediction before biopsy was not reliable. These nodules had the four biopsy-recommendation patterns described earlier, such as isoechoic nodule with a surrounding halo or refractive edges, which came to be simplied in our series as isoechoic nodules with or without a halo (types 7 and 8). A hypoechoic nodule with or without central microcalcication or with central macrocalcication in other series [25, 26, 32], for which biopsy was recommended, was the most worrisome pattern (type 6) in our study. We identied other common patterns, including the type 5 red light pattern, or an intensely hypervascular lesion that on Doppler 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-re nodules with intense peripheral vascularity and nodules described as other (type 10), which did not t any of the classic patterns. Calcication, although commonly seen in nodules requiring biopsy, was never seen as an isolated nding. The likelihood of benignity of these nodules (type 510) ranged from 60% (type 9, ring of re) to 91% (type 10, other). Because of this lack of predictability, we believed that these nodules should be considered 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 ndings, the retrospective nature of the study, and the fact that nodule characterization was dependent 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 biopsies will be chosen prospectively in the weeks before their performance, and the images will be shown to these readers, who will decide whether biopsy should be performed. Analysis of interobserver variability for assigning nodules to a specic pattern will be analyzed, as will the characterizations with nal 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. Specic morphologic patterns are highly predictive of benignity. Specically, a nodule that has a uniform nonhypervascular spongiform appearance, is a cystic lesion with a colloid clot, has a giraffelike pattern, or is diffusely hyperechoic can be observed rather than biopsied. If, conversely, 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
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