Likelihood of malignancy in thyroid nodules according to a proposed Thyroid Imaging Reporting and Data System (TI-RADS) classification merging suspicious and benign ultrasound features

Delfim, Ricardo Luiz Costantin; Veiga, Leticia Carrasco Garcez da; Vidal, Ana Paula Aguiar; Lopes, Flávia Paiva Proença Lobo; Vaisman, Mário; Teixeira, Patrícia de Fatima dos Santos

doi:10.1590/2359-3997000000262

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Archives of Endocrinology and Metabolism

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Original Articles • Arch. Endocrinol. Metab. 61 (3) • May-Jun 2017 • https://doi.org/10.1590/2359-3997000000262 copy

Likelihood of malignancy in thyroid nodules according to a proposed Thyroid Imaging Reporting and Data System (TI-RADS) classification merging suspicious and benign ultrasound features

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objective

The aim of this study was to describe the ultrasound features of benign and malignant thyroid nodules and evaluate the likelihood of malignancy associated with each feature according to the Bethesda System for Reporting Thyroid Cytopathology and histopathology. With this analysis, we propose a new TI-RADS classification system.

Materials and methods

The likelihood of malignancy from ultrasound features were assessed in 1413 thyroid nodules according to the Bethesda System for Reporting Thyroid Cytopathology and histopathological findings. A score was established by attributing different weights to each ultrasound feature evaluated.

Results

Features positively associated with malignancy in bivariate analysis received a score weight of +1. We attributed a weight of +2 to features which were independently associated with malignancy in a multivariate analysis and +3 for those associated with the highest odds ratio for malignancy (> 10.0). Hence, hypoechogenicity (graded as mild, moderate or marked, according to a comparison with the overlying strap muscle), microcalcification and irregular/microlobulated margin received the highest weights in our scoring system. Features that were negatively associated with malignancy received weights of -2 or -1. In the proposed system a cutoff score of 2 (sensitivity 97.4% and specificity 51.6%) was adopted as a transition between probably benign (TI-RADS 3) and TI-RADS 4a nodules. Overall, the frequency of malignancy in thyroid nodules according to the categories was 1.0% for TI-RADS 3, 7.8% for TI-RADS 4a, 35.3% for TI-RADS 4b, and 84.7% for TI-RADS 5.

Conclusion

A newly proposed TI-RADS classification adequately assessed the likelihood of malignancy in thyroid nodules.

Thyroid nodules; TI-RADS; thyroid cancer

Ultrasound features		Definition
Composition	Solid appearance	> 90% of nodule component is solid (24)
Composition	Spongiform appearance	Predominantly cystic with multiple degenerative areas (> 50% in its composition) (25)
Grade of echogenicity of the solid component	Hyperechogenicity	Echogenicity greater than thyroid parenchyma (10,11,25,27)
	Hypoechogenicity (any degree)	Echogenicity lesser than thyroid parenchyma (28,29), including thyroid nodules with mild, moderate* and marked *** hypoechogenicity (30)
	Moderate to marked hypoechogenicity	Echogenicity similar and lesser than that of strap muscle, including thyroid nodules with moderate and marked* hypoechogenicity
	Marked hypoechogenicity	Echogenicity lesser than that of strap muscle (30)
Margins and halos	Absence of a halo	No identified hypoechogenic halo
	Irregular thick halo	Irregular halo, ≥ 2 mm in thickness (26)
	Regular thin halo	Complete and regular, < 2 mm in thickness (26)
	Irregular/microlobulated margin	Irregular or microlobulated margins (8,9,21,30)
	Blurred margin	Not well defined margin (31)
Presence of different hyperechogenic spots, including any kind of calcifications	Microcalcification	Peripheral and/or inner microcalcification, defined by hyperechogenic spot ≤ 2 mm, either with or without acoustic shadow (26)
	Macrocalcification	Peripheral and/or inner hyperechogenic coarse or spot > 2 mm, either with or without acoustic shadow (26)
	Egg shell calcification	Complete and regular calcification border (5,8,25)
	Colloid Crystal	Hyperechogenic spot with comet-tail artifact (birefringence) (29,32)
	Unspecific hyperechoic spots	Hyperechogenic spot without acoustic shadow or comet-tail artifact that is not well characterized as calcification or colloid crystal (29,31)
Shape	Non-ovoid shape	Anteroposterior diameter greater than its transverse or longitudinal one
Shape	Taller-than-wide shape	Anteroposterior diameter greater than its transverse diameter (30)
Doppler color flow	Any degree of central flow	Any degree of central flow (28,33)
Doppler color flow	Predominant central flow	Central flow greater than peripheral blood flow and exclusively central flow (34)

Ultrasound features	Frequency distribution of ultrasound features according to the Bethesda system (%)				Relationship each ultrasound feature with cytopathological and histopathological assessments

	Bethesda system categories #				Benign and suspicious/malignant cytopathology (n = 1413)				Subgroup of nodules with histopathological assessment (n = 338)

	II	V	VI	p value	Bivariate analysis*	p value	Multivariate analysis*	p value	Bivariate analysis*	p value	Multivariate analysis*	p value
Solid appearance	48.5 (n = 567)	92.3 (n = 143)	92.0 (n = 77)	< 0.001	12.3 (7.6-19.9)	< 0.001	5.14 (2.8-9.4)	< 0.001	10.2 (4.5-18.9)	< 0.001	3.9 (1.5-9.7)	0.04
Hypoechogenicity (any degree)	34.2 (n = 401)	93.5 (n = 145)	93.0 (n = 78)	< 0.001	26.8 (15.8-45.0)	< 0.001	4.7 (2.4-9.4)	< 0.001	22.3 (11.7-42.8)	< 0.001	4.3 (1.7-11.1)	0.02
Marked hypoechogenicity	12.9 (n = 149)	63.0 (n = 97)	73.5 (n = 61)	< 0.001	8.8 (5.8-13.5)	< 0.001			9.9 (3.0-32.6)	< 0.001
Moderate to marked hypoechogenicity	3.7 (n = 43)	26.5 (n = 41)	22.6 (n = 19)	< 0.001	13.5 (9.8-18.6)	< 0.001	3.45 (2.0-9.0)	< 0.001	13.2 (6.9-25.2)	< 0.001	3.43 (1.3-9.2)	0.01
Irregular/microlobulated margin	0.7 (n = 8)	34.8 (n = 54)	40.5 (n = 34)	< 0.001	84.5 (40.2-178)	< 0.001	28.8 (10.9-75.9)	< 0.001	56.1 (7.7-409)	0.001
Blurred margin	11.7 (n = 136)	16.6 (n = 25)	27.4 (n = 23)	< 0.001	1.9 (1.3-2.8)	< 0.001	0.38 (0.2-0.8)	0.009	1.8 (0.9-3.76)	0.147
Absence of a halo	77.5 (n = 504)	90.9 (n = 140)	86.9 (n = 73)	< 0.001	2.5 (1.6-3.8)	< 0,001			3.2 (1.7-5.9)	< 0.001
Irregular/thick halo	0.6 (n = 7)	2.6 (n = 4)	1.2 (n = 1)	0.09	3.5 (1.0-11.3)	0.05			1.0 (1.0-1.01)	0.628
Microcalcification	2.1 (n = 25)	39.0 (n = 60)	52.4 (n = 44)	< 0.001	35.6 (22.2-57.1)	< 0.001	12.6 (6.3-25.2)	< 0.001	24.8 (17.6-80.6)	0.001	12.0 (2.6 -54.5)	0.01
Taller-than-wide	8.7 (n = 101)	8.0 (n = 14)	19.8 (n = 18)	0.020	1.5 (0.9-2.4)	0.58			2.3 (0.9-5.7)	0.07
Non-ovoid shape	9.0 (n = 104)	9.0 (n = 14)	18.1 (n = 15)	0.026	1.4 (0.9-2.2)	0.06			4.1 (1.2-13.8)	0.015
Any degree of central flow	71,1 (n = 820)	66.0 (n = 95)	72.3 (n = 60)	0.424	0.9 (0.6-1.2)	0.40			0.7 (0.3-1.1)	0.10
Predominantly central flow	3.2 (n = 37)	14.2 (n = 22)	11.9 (n = 10)	0.001	4.7 (2.9-7.8)	< 0.001	2.28 (1.2-5.1)	0.045	3.4 (1.2-9.9)	0.02
Spongiform appearance	2.0 (n = 24)	0	0	0.083	0.98 (0.97-0.98)	0.001			0.98 (0.95-1.0)	0.08
Eggshell calcification	0.2 (n = 2)	0	0	0.467	0.99 (0.99-1.0)	0.648			N.E.**	N.E.**
Colloid Crystal	2.3 (n = 27)	0	0	0.062	0.97 (0.96-0.99)	0.01			0.41 (0.03-6.7)	0.253
Hyperechogenicity	2.6 (n = 30)	0	0	0.044	0.97 (0.96-0.98)	0.04			0.98 (0.95-1.0)	0.08
Thin regular halo	21.9 (n = 256)	7.1 (n = 11)	11.9 (n = 10)	< 0.001	0.34 (0.2-0.55)	< 0.001			0.25 (0.13-0.49)	0.001
Hyperechoic spot	7.2 (n = 84)	12.9 (n = 20)	9.5 (n = 8)	0.057	1.7 (1.1-2.7)	0.03	4.01 (2.2-7.4)	< 0.001	1.22 (0.5-2.7)	0.388	3.1 (1.1-8.3)	0.03
Macrocalcification	4.2 (n = 49)	14.2 (n = 22)	16.7 (n = 14)	< 0.001	4.0 (2.6-6.4)	0.001			2.2 (0.9-5.1)	0.122

Ultrasound features	Weight conception process	Score
Marked hypoechogenicity	This feature alone was not independently associated with a likelihood of malignancy in multivariate analysis and received initially a score weight of +1. However, the weight of this feature increased since it is also included in the feature of hypoechogenicity of any degree (+2) and in moderate to marked hypoechogenicity (+2). The sum of all these weights resulted in the value of +5, attributed here	+5
Moderate hypoechogenicity	The presence of moderate to marked hypoechogenicity was independently associated with the likelihood of malignancy and received a weight of +2. However, the weight of this feature increased it is also included in the feature of hypoechogenicity of any degree (+2), yielding a score weight of +4. Moderate to marked hypoechogenicity term was replaced to “moderate hypoechogenicity”, as marked hypoechogenicity has its own score	+4
Microcalcification	Independently associated with the likelihood of malignancy (OR > 10.0)	+3
Irregular/microlobu lated margin	Independently associated with the likelihood of malignancy (OR > 10.0)	+3
Mild hypoechogenicity	This degree of hypoechogenicity received a weight based only on the feature of hypoechogenicity of any degree which did not meet the criteria for moderate or marked hypoechogenicity; it was then attributed a weight of +2 since it was included in the overall group of any degree hypoechoic nodules	+2
Solid appearance	Independently associated with the likelihood of malignancy (OR > 1.0 and ≤ 10.0)	+2
Undefined hyperechoic spot	Independently associated with the likelihood of malignancy (OR > 1.0 and ≤ 10.0)	+2
Predominantly central flow	Independently associated with the likelihood of malignancy (OR > 1.0 and ≤ 10.0)	+2
Non-ovoid shape	Ultrasound features positively associated with the likelihood of malignancy in bivariate but not multivariate analysis	+1
Macrocalcification		+1
Absence of a halo		+1
Irregular/thick halo		+1
Regular thin halo	Ultrasound features negatively associated with the likelihood of malignancy in bivariate but not multivariate analysis	-1
Crystal colloid		-1
Hyperechogenicity		-1
Spongiform appearance		-1
Blurred margin	Negatively and independently associated with the likelihood of malignancy	-2

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[1] Correspondence to: Ricardo Luiz Costantin Delfim. Av. Professor Rodolpho Rocco, 255. Hospital Universitário. Clementino Fraga Filho. Cidade Universitária. 21941-913 – Rio de Janeiro, RJ, Brasil. dr.ricardodelfim@gmail.com