MATERIALS AND METHODS. From a registry of the records of 1,232 fne-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 identifed for whom both a pathology report and ultrasound images were available.
From the alphabetized list generated, the frst 500 nodules were reviewed. We analyzed the accuracy of individua
sonographic features and of 10 discrete recognizable morphologic patterns in the prediction of benign histologic
fndings.
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 identifcation o
benign nodules. Four specifc patterns were identifed: spongiform confguration, cyst with colloid clot, giraffe
pattern, and diffuse hyperechogenicity, which had a 100% specifcity for benignity. In our series, identifcation of
nodules with one of these four patterns could have obviated more than 60% of thyroid biopsies.
CONCLUSION. Recognition of specifc 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
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.
AJ R 2009; 193:207213
0 361 8 03 X/ 0 9 /1 9 3 1 2 0 7
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2007, the cases of 650 patients (436 women, All diagnostic ultrasound examinations
The fnal diagnosis was based on the
64 men; average age, 54.7 years; range, 17 and FNA biopsies were performed with an cytologic result; fnal pathologic confrmation
88 years) were identifed in which both
Acuson 300 or Antares unit (both Siemens was limited to the 20 malignant tumors
pathology reports and ultrasound images
Healthcare). All FNA biopsies were
resected. In the 20 patients with these
were available. From the alphabetized list performed by a group of four cytologists
tumors, there was no discrepancy between
generated, the frst 500 nodules were
(average experience, 5 years) under
the initial cytologic and the fnal pathologic
reviewed. This HIPAA-compliant study was ultrasound guidance by one of fve
result. The cytologic results were divided
approved by our institutional review board radiologists (average experience, 20.5
into three categories: 1, benign nodules,
with a waiver of informed consent. We
years). The biopsies were performed with including colloid nodules, hyperplastic
analyzed the accuracy of individual
25-gauge spinal needles in most instances; a nodules, and localized thyroiditis; 2,
sonographic features and of 10 discrete
27-gauge needle was used for hypervascular intermediate nodules, including follicular
recognizable morphologic patterns in the
lesions. At least two passes were made for and Hrthle cell neoplasms; and 3,
prediction of benign histologic fndings.
each nodule (average, 3.2 passes per nodule; carcinoma. Type 1 nodules were determined
range, 26 passes). All specimens
to be nodules that did not require biopsy;
types 2 and 3 were nodules requiring biopsy.
Bonavita et al.
Ultrasound Technique
were evaluated immediately by the
cytologists to confrm sample adequacy.
Data Analysis
Fig. 1Individual
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-defned borders. C, 36year-old man with
papillary carcinoma.
Ultrasound scan shows
microcalcifcations (a r ro
w ), which are easily
confused with comet-tail
shadowing. Important
fnding is
hypoechogenicity of
nodule. D, 37-year-old
woman with medullary
carcinoma. Ultrasound
scan shows
macrocalcifcation. E, 37year-old woman with
papillary carcinoma.
Color Doppler
ultrasound image shows
hypervascular nodule.
DE
208 AJR:193, July 200
Thyroid Ultrasound
TABLE 1: Diagnostic Characteristics of Each Classification in Identification of Benign Masses
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Classifiation Sensitivity (%) Specifcity (%) 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 calcifcation 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 confguration 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 classifcation 14 100.0 (40/40) 65.9 (303/460) 20.3 (40/197) 100.0 (303/303) < 0.000
1NoteValues in parentheses are numbers
of nodules.
Bonavita et al.
AC
BD FE
GI
H phologic patterns. A, 41-year-old man with colloid nodule. Ultrasound scan shows spongiform nodule. Similarity of
J nodule to water-flled sponge is evident. B, 52-year-old man with colloid cyst. Ultrasound scan shows cyst with colloid
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F
i
g
.
2
M
o
r
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 microcalcifiations (a r ro w s ) 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 fre, or peripheral hypervascularity. J, 61-year-old man with colloid nodule. Ultrasound scan shows
nodule that fts into no other pattern.
Thyroid Ultrasound
TABLE 3: Features of Morphologic Types of Thyroid Nodules
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Pattern Texture Vascularity Margins Densities 1, Spongiform or puff pastry Spongiform internal cysts None or
isovascular Well-defned Present or absent comet tail 2, Cyst with colloid clot Cystic with mural clot None or isovascular Welldefned 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-defned 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 Welldefned Present or absent 9, Ring of fre Any Peripheral hypervascularity Well-defned 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 Hashimotos 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 fre 6 5 0 1 4 4 0 10, Other 11 10 1 0 1 0 1
NotePatterns 14 are invariably associated with benign conditions. Patterns 510 are variable
.detection of malignancy.
The persistent combination of some Like Reading et al. [23], we found
Bonavita et al.
TABLE 5: Patterns of Nodules That Do Not Require Biopsy Versus Patterns of Reading et al. [23]
Current Study Classifcation 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-flled cystic nodules; 3, large predominantly cystic
nodule 3, Giraffe 4, Diffuse, multiple small hypoechoic nodules with intervening echogenic bands indicative of Hashimotos
thyroiditis 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 microcalcifcations; 2, coarse calcifcations in a
hypoechoic nodule 7, Isoechoic without halo 4, Solid mass with refractive shadowing from the edges, believed to be due to
fbrosis 8, Isoechoic with halo 3, Well-marginated, ovoid, solid nodule with a thin hypoechoic halo 9, Ring of fre, peripheral
vascularity 10, Othe
rwere also colloid nodules. If the
We identifed other common patterns, who will decide whether biopsy should
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We conclude that biopsy of a large should be performed regardless of the year follow-up. Radiology 2000; 215:801
806
number of thyroid nodules (in our
individual features or pattern of the
4. Jemal A, Murray T, Ward E, et al. Cancer
study, 61%) can be avoided when a
nodule.
statistics, 2005. CA Cancer J Clin 2005;
pattern approach to nodule
55:1030 [Erratum in CA Cancer J Clin
characterization is used. Specifc
References
2005; 55:259]
morphologic patterns are highly
1. Ezzat S, Sarti DA, Cain DR, et al. Thyroid
predictive of benignity. Specifcally, a incidentalomas: prevalence by palpation and 5. Harnsberger H. Diagnostic imaging:
head and neck. Salt Lake City, UT: Amirsys,
nodule that has a uniform
ultrasonography. Arch Intern Med 1994;
2004:2440
154:18381840
nonhypervascular spongiform
6. Kountakis SE, Skoulas IG, Maillard AA.
appearance, is a cystic lesion with a
2. Frates MC, Benson CB, Charboneau JW,
The radiologic work-up in thyroid surgery:
et
al.
Management
of
thyroid
nodules
colloid clot, has a giraffelike pattern, or
fne-needle biopsy versus scintigraphy and
detected at US: Society of Radiologists in
is diffusely hyperechoic can be
ultrasound. Ear Nose Throat J 2002; 81:151
Ultrasound
consensus
conference
statement.
observed rather than biopsied. If,
154
Radiology 2005; 237:794 800
conversely, a nodule does not
7. Rago T, Vitti P, Chiovato L, et al. Role
3. Brander AE, Viikinkoski VP, Nickels JI, of conventional ultrasonography and
correspond to one of these four
color flw-Doppler sonography in
patterns, according to our data biopsy Kivisaari LM. Importance of thyroid
abnormalities detected at US screening: a 5- predicting malignancy in cold
Down
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www.
ajronli
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73.83
on
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from
IP
addres
s
36.79.
73.83.
Copyr
ight
ARRS
. For
perso
nal
use
only;
all
rights
reserv
ed
thyroid nodules. Eur J Endocrinol 1998; 16. Frates MC, Benson CB, Doubilet PM, 23. Reading CC, Charboneau JW, Hay ID,
138:4146 8. Giuffrida D, Gharib H.
et al. Prevalence and distribution of
Sebo TJ. Sonography of thyroid nodules: a
Controversies in the mancarcinoma in patients with solitary and
classic pattern diagnostic approach.
agement of cold, hot, and occult thyroid multiple thyroid nodules on Thyroid
Ultrasound Q 2005; 21:157 165
nodules. Am J Med 1995; 99:642650 Ultrasound
24. Hegedus L. Thyroid ultrasound.
9. Papini E, Guglielmi R, Bianchini A, et
Endocrinol Metab Clin North Am 2001;
al. Risk of malignancy in nonpalpable
30:339360
sonography. J Clin Endocrinol Metab
thyroid nodules: predictive value of
25. Hoang JK, Lee WK, Lee M, Johnson D,
2006; 91: 34113417
ultrasound and color-Doppler features. J
Farrell S. US features of thyroid malignancy:
17. Cooper DS, Doherty GM, Haugen BR,
Clin Endocrinol Metab 2002; 87:1941
pearls and pitfalls. RadioGraphics 2007;
et al. Management guidelines for patients
1946
27:847860
with thyroid nodules and differentiated
10. Jun P, Chow LC, Jeffrey RB. The
thyroid cancer. Thyroid 2006; 16:109142 26. Takashima S, Fukuda H, Nomura N,
sonographic features of papillary thyroid
Kishimoto H, Kim T, Kobayashi T. Thyroid
carcinomas: pictorial essay. Ultrasound Q 2005; 18. Pacini F, Schlumberger M, Dralle H,
nodules: reevaluation with ultrasound. J Clin
Elisei R, Smit JW, Wiersinga W; European
21:3945
Ultrasound 1995; 23:179184
Thyroid Cancer Taskforce. European
11. Kim EK, Park CS, Chung WY, et al.
27. Vandermeer FQ, Wong-You-Cheong J.
consensus for the management of patients
New sonographic criteria for recommending
with differentiated thyroid carcinoma of the Thyroid nodules: when to biopsy. Appl Radiol
fne-needle aspiration biopsy of nonpalpable
follicular epithelium. Eur J Endocrinol 2006; 2007; 36:819
solid nodules of the thyroid. AJR 2002;
154:787803
28. Pacini F, Burroni L, Ciuoli C, Di
178:687691
19. British Thyroid Association and Royal Cairano G, Guarino E. Management of
12. Koike E, Noguchi S, Yamashita H, et al.
thyroid nodules: a clinicopathological,
College of Physicians. Guidelines for the
Ultrasonographic characteristics of thyroid
evidence-based approach. Eur J Nucl Med
management of thyroid cancer in adults.
nodules: prediction of malignancy. Arch
London, UK: Publication Unit of the Royal Mol Imaging 2004; 31:14431449
Surg 2001; 136: 334337
College of Physicians, 2002
29. Castro MR, Gharib H. Thyroid fne13. Chan BK, Desser TS, McDougall IR, et al.
20. Rodrigues FJ, Limbert ES, Marques AP, needle aspiration biopsy: progress, practice,
Common and uncommon sonographic features
et al.; Grupo de Estudo da Tiride. Treatment and pitfalls. Endocr Pract 2003; 9:128136
of papillary thyroid carcinoma. J Ultrasound
and follow up protocol in differentiated
30. Ross DS. Nonpalpable thyroid nodules:
Med 2003; 22:10831090
thyroid carcinomas of follicular origin [in
managing an epidemic. J Clin Endocrinol
14. Ahuja A, Chick W, King W, Metreweli Portuguese]. Acta Med Port 2005; 18:216 Metab 2002; 87: 19381940
C. Clinical signifcance of the comet-tail
21. Societ Italiana di Endocrinologia,
31. Sahin M, Sengul A, Berki Z, Tutuncu
artifact in thyroid ultrasound. J Clin
Associazione Italiana di Medicina Nucleare NB, Guvener ND. Ultrasound-guided fneUltrasound 1996; 24:129133
ed Imaging Molecolare, Associazione
needle aspiration biopsy and
15. Kovacevic DO, Skurla MS. Sonographic Italiana di Fisica Medica. Linee Guida SIE- ultrasonographic features of infracentimetric
diagnosis of thyroid nodules: correlation with AIMN-AIFM per il trattamento e follow-up nodules in patients with nodular goiter:
the results of sonographically guided fnedel carcinoma tiroideo differenziato della correlation with pathological fndings.
needle aspiration biopsy. J Clin Ultrasound tiroide. Rome, Milan, and Gazzada, Italy: Endocr Pathol 2006; 17:6774
2007; 35:6367
SIE, AIMN, and AIFM, 2004:175
32. Iannuccilli JD, Cronan JJ, Monchik
22. Van De Velde CJ, Hamming JF, Goslings JM. Risk for malignancy of thyroid
nodules as assessed by sonographic
BM, et al. Report of the consensus
development conference on the management criteria: the need for biopsy. J Ultrasound
Med 2004; 23:1455146
of differentiated thyroid cancer in The
Netherlands. Eur J Cancer Clin Oncol 1988;
24:287292
4AJR:193, July 2009 213