ORIGINAL ARTICLE

Computed Tomography Features of Papillary Thyroid Carcinomas Dong Wook Kim, MD Objective: No previous study has been reported on computed tomography (CT) features of papillary thyroid carcinoma (PTC). This study aimed to evaluate CT features of PTCs and to compare the ultrasound (US) and CT features of PTCs. Methods: This study enrolled 134 consecutive PTC patients who received neck US and CTexaminations before thyroid surgery. For each case, US and CT features were retrospectively and independently investigated by a single radiologist using a picture archiving and communication system. Results: Of the 120 PTC cases, 106 were detected by CT, but 14 were not visualized. In each CT category, the most common feature included low attenuation, homogeneous attenuation, a taller-than-wide shape, no calcifications, decreased enhancement, and homogeneous enhancement. In the comparison of US and CT features, nodular shape and calcification demonstrated a statistically significant difference (P < 0.05), but no significant difference existed in the nodular margin (P = 0.559). For the 21 PTCs with ultrasonographically detected microcalcifications, CT showed no calcifications. Conclusions: The study results demonstrated that the most common CT features of PTCs included homogenous low attenuation, a taller-thanwide shape, no calcifications, and homogeneous decreased enhancement and that CT was inferior to US for evaluating nodular shape and calcification. Key Words: thyroid, papillary thyroid carcinoma, computed tomography, ultrasound, malignancy (J Comput Assist Tomogr 2014;38: 936–940)

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urrently, ultrasound (US) is the accepted method for the first diagnostic evaluation of the thyroid.1–3 Known US features of malignant thyroid nodules include marked hypoechogenicity, an irregular (or spiculated) margin, a taller-than-wide shape, and microcalcifications.1–5 However, US has several limitations, and its most important limitation is operator dependency.1,3 Unlike US, computed tomography (CT) does not have the limitation of operator dependency. Furthermore, the incidental detection of thyroid nodules in neck CT is common, but consecutive US examination has been applied for further evaluation because of limited information on CT characteristics for differentiating malignant and benign thyroid nodules.6–8 Although the prevalence of thyroid cancers depends on the region, the most common type of thyroid cancer worldwide is papillary thyroid carcinoma (PTC).2,3 Furthermore, the prevalence of thyroid cancer has been rapidly increasing in South Korea, but the reason is unknown.9,10 Although numerable US studies have been published, to the best of my knowledge, no previous study has reported the CT features for the detection of

From the Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea. Received for publication May 26, 2014; accepted July 31, 2014. Reprints: Dong Wook Kim, MD, Department of Radiology, Busan Paik Hospital, Inje University College of Medicine, Busan, South Korea, 614-734 (e‐mail: [email protected], [email protected]). The author declares no conflict of interest. Copyright © 2014 by Lippincott Williams & Wilkins

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PTC. Therefore, the purpose of this study was to assess CT features of PTC and to compare the US and CT features of PTCs in patients who underwent thyroid surgery.

MATERIALS AND METHODS Study Population This retrospective study was approved by the institutional review board before subject selection, and informed consent was waived. From July 2013 to December 2013, 134 patients with PTC (116 women and 18 men; average age, 48.3 ± 10.2 years; age range, 19–76 years) sequentially underwent preoperative neck US and CT examinations before thyroid surgery. Inclusion criteria for this study were as follows: the primary condition for inclusion was a PTC nodule, along with matching indications for both imaging and histopathologic findings. Exclusion criteria included poor US and CT image quality. Finally, 14 patients (14 women; average age, 50.3 ± 14.5 years; age range, 19–70 years) were excluded from this study.

US and CT For neck US examination, a high-resolution US instrument (iU 22; Philips Medical Systems, Bothell, Wash) equipped with a 5- to 12-MHz linear probe was used. Neck CT scans were conducted using a contrast medium (130 mL iopamidol [Pamiray 370]; Dongkook Pharm, Seoul, South Korea; 2.5 mL/s; delay, 45 seconds) and a 64-channel multidetector CT scanner (Aquilion One; Toshiba Medical System, Otawara, Japan) or a 128-channel multidetector CT scanner (LightSpeed; General Electric Medical System, Milwaukee, Wis). Nonenhanced axial, contrastenhanced axial, and contrast-enhanced coronal reformatted CT images were acquired for all cases (slice thickness, 3 mm; reconstruction increment, 3 mm). The time interval between preoperative neck CT and subsequent thyroid surgery was less than 4 weeks.

Image Analysis A single radiologist with 12 years’ experience in neck US and CT interpretations investigated the imaging features using a picture archiving and communication system. The imaging features for the US and CT examinations were independently analyzed under blinded conditions for each imaging result. For the PTCs, the US features were analyzed based on the echogenicity, margin, shape, pattern of calcifications, and vascularity of the nodules.1–5 Nodule echogenicity was classified according to a comparison with the adjacent parenchyma and strap muscle as follows: isoechogenicity (defined as the same echogenicity, as compared with the adjacent normal thyroid parenchyma), hypoechogenicity (defined as decreased echogenicity, as compared with the adjacent normal thyroid parenchyma, and increased echogenicity, as compared with the strap muscle), marked hypoechogenicity (defined as the same or decreased echogenicity, as compared with the strap muscle), hyperechogenicity (including complete calcification with marked

J Comput Assist Tomogr • Volume 38, Number 36, November/December 2014

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J Comput Assist Tomogr • Volume 38, Number 36, November/December 2014

CT Features of PTC

hyperechogenicity and posterior shadowing), and anechoic (ie, thyroid cyst). The PTC margins included smooth, irregular (including spiculated margin), and lobulated types. According to the nodular shape, PTCs were classified as an ovoid (anteroposterior diameter/transverse diameter ratio and anteroposterior diameter/longitudinal diameter ratio ≤0.8), round, or taller-than-wide shape (anteroposterior diameter/transverse diameter ratio or anteroposterior diameter/ longitudinal diameter ratio >1). Based on the degrees and patterns of nodular calcification, the nodule was classified as none, punctate (microcalcifications), rim (eggshell), nodular, complete, and mixed (punctuate plus nodular). On the basis of a color Doppler US, PTCs were divided as follows: no or scant vascularity, peripheral predominance, central predominance, and mixed vascularity. The CT features of the PTCs were investigated based on the composition, CT attenuation degree and pattern, margin, shape, pattern of calcification, and degree and pattern of parenchymal enhancement. For determining the degrees of CT attenuation and enhancement of thyroid nodules, the adjacent thyroid parenchyma was utilized as a reference, and complete calcification was classified as high attenuation. Both CT attenuation and enhancement of thyroid nodules were categorized as homogeneous, inhomogeneous, and heterogeneous patterns. Like US features, the margin of the thyroid nodules was classified as smooth, irregular, or lobulated, and the shape of the thyroid nodules was divided into ovoid, round, or taller-than-wide according to the ratio of anteroposterior and transverse diameters measured in contrast-enhanced CT images. On the basis of the degrees and patterns of nodular calcification, the nodule was classified as none, punctate, rim, nodular, complete, and mixed (punctate plus nodular).

diameter for the primary PTCs was 9.4 ± 5.9 mm that was measured on a histopathology specimen. The location of the primary PTCs included right thyroid (n = 59), left thyroid (n = 52), and isthmus (n = 9). The type of thyroid surgery included total thyroidectomy (n = 64), subtotal thyroidectomy (n = 5), and lobectomy (n = 51). Histopathologic results for the thyroid parenchyma included normal (n = 83), Hashimoto thyroiditis (n = 4), and non– Hashimoto lymphocytic thyroiditis (n = 33). The frequencies of the individual US features for PTCs in 120 patients are summarized in Table 1. All cases were classified according to the number of 4 malignant US features as follows: none (n = 8), 1 (n = 34), 2 (n = 29), 3 (n = 36), and 4 (n = 13) (Fig. 1). The 8 cases with no malignant US features had complete calcification (n = 2), isoechogenicity (n = 4), and hypoechogenicity (n = 2). Of the 4 isoechogenicity cases, 2 had the follicular variant of PTC (Fig. 2). With individual US features, the most common feature in each category included marked hypoechogenicity, an irregular margin, a taller-than-wide shape, no calcifications, and no or scant vascularity. With nodular vascularity, the prevalence rate for centrally predominant vascularity was only 10.8% (13/120). The frequencies of the individual CT features for PTCs in 120 patients are summarized in Table 2. Of the 120 PTC cases, 106 (nodule size range, 4.1–42.1 mm; mean size, 10.0 ± 5.9 mm) were detected by CT, but 14 (nodule size range, 3.1– 6.8 mm; mean size, 4.6 ± 1.1 mm) were not visualized (Fig. 3). Of the 14 nonvisualized cases by CT, the histopathologic results for the thyroid parenchyma included normal (n = 6), Hashimoto

Histopathology of Thyroid Parenchyma

US Features

Papillary thyroid carcinoma has characteristic nuclear features including an enlarged, oval, or elongated shape and an overlapping, clearing, and irregular nuclear contour including grooves and pseudoinclusions. A papillary architecture is not a required feature for the diagnosis of the PTC. The follicular variant of PTC is entirely composed of follicles with no papillary structures, and the lining cells have the same nuclear features as typical papillary carcinoma. Histopathologic findings of thyroid parenchyma were classified by a single pathologist as follows: Hashimoto thyroiditis showed progressive loss of thyroid follicular cells with replacement by lymphocytes and formation of germinal centers associated with fibrosis. Non–Hashimoto lymphocytic thyroiditis displayed diffuse infiltration of the thyroid gland with lymphocytes and other inflammatory cells but none of the typical histopathologic features of Hashimoto thyroiditis, such as oxyphilic metaplasia, follicular atrophy, and follicular disruption. The normal thyroid parenchyma showed no visual evidence of coexisting, diffuse thyroid disease.

Echogenicity Isoechoic Hypoechoic Marked hypoechoic Hyperechoic Anechoic Margin Smooth Irregular (spiculated) Lobulated Shape Ovoid Round Taller-than-wide Calcification None Microcalcifications Rim (eggshell) Nodular Complete Mixed (micro- and macro-) Vascularity No/scant Peripheral Central Mixed

Statistical Analysis The Pearson χ2 test was used to compare the prevalence of individual features between US and CT. Statistical analyses were performed using SPSS for Windows (version 17.0.1; SPSS Inc, Chicago, Ill), and a P < 0.05 was considered statistically significant.

RESULTS Of the 120 patients (102 women and 18 men; average age, 48.1 ± 9.6 years; age range, 27–76 years), the mean largest © 2014 Lippincott Williams & Wilkins

TABLE 1. Frequency Analysis of US Features of Papillary Thyroid Carcinomas in 120 Patients

6 (5) 12 (10) 99 (82.5) 3 (2.5) 0 (0) 37 (30.8) 63 (52.5) 20 (16.7) 33 (27.5) 39 (32.5) 48 (40) 68 (56.7) 34 (28.3) 5 (4.2) 3 (2.5) 1 (0.8) 9 (7.5) 76 (63.3) 2 (1.7) 13 (10.8) 29 (24.2)

Data are number of cases, with percentage in parentheses.

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Kim

FIGURE 1. Ultrasound and CT features of primary PTC in the right midthyroid in a 51-year-old woman (largest diameter, 11.8 mm). A and B, In transverse (A) and longitudinal (B) gray-scale sonograms of the right thyroid, a PTC (arrows) has marked hypoechogenicity, an irregular margin, and microcalcifications (arrowheads). C and D, In axial nonenhanced (C) and enhanced (D) CT images, a PTC (arrows) in the right thyroid shows homogeneous low attenuation, a smooth margin, a round shape, no calcifications, and homogeneous decreased enhancement. The thyroid parenchyma was normal in histopathology.

thyroiditis (n = 2), and non–Hashimoto lymphocytic thyroiditis (n = 6). The PTCs had an entirely solid composition by CT. As for the individual CT features, the most common feature in each category included low attenuation, homogeneous attenuation, a taller-than-wide shape, no calcifications, decreased enhancement, and homogeneous enhancement. In the nodular margin, smooth and irregular margins had a similar prevalence, but there was no predominant feature. A comparison of nodular margin, shape, and calcifications between US and CT in 106 PTC patients is listed in Table 3. Nodular shape and calcification showed a statistically significant difference (P < 0.05), but there was no significant difference in nodular margin (P = 0.559). As for the PTC margin, the prevalence of a lobulated margin was similar for both modalities, whereas those of smooth and irregular margins were different; the prevalence of a smooth margin was higher with CT, whereas the prevalence of an irregular margin was higher with US. Meanwhile, regarding the PTC shape, the prevalence of a taller-thanwide shape was higher with CT, whereas the prevalence of ovoid and round shapes was higher with US. Furthermore, the overall detection rate with CT for PTC calcification was lower than that of US. Of the 21 PTCs, US revealed microcalcifications, whereas CT showed no calcifications (Fig. 1).

DISCUSSION A neck CT is a popular imaging tool for evaluating various neck lesions because it has many advantages such as a wide field of view, objectivity, and a detailed display of bone or aircontaining organs.11 In thyroid cancer patients, the use of neck CT has been restricted in preoperative tumor-node-metastasis staging because of radiation hazards. However, incidental thyroid nodules are frequently found on cross-sectional imaging of the neck in patients being examined for other reasons.6–8,12 It is possible that the workup cost of incidental thyroid nodules includes unnecessary patient anxiety and a substantial health care economic burden.6,13 Nevertheless, the specific CT features for PTCs can be helpful for the management of incidental thyroid nodules. In the current study, the most common PTC features with CT included a homogeneously low attenuation, a taller-thanwide shape, no calcifications, and a homogeneously decreased enhancement. Based on a comparison with previous studies,7,8,12 low attenuation, homogeneous attenuation, no calcifications, and homogeneous enhancement are commonly observed in both benign and malignant solid thyroid nodules, whereas a tallerthan-wide shape and decreased enhancement may not be common in benign solid thyroid nodules. For clarity, a comparison study is

FIGURE 2. Ultrasound and CT features of primary PTC in the right lobe in a 36-year-old woman (largest diameter, 42.1 mm). A and B, In transverse (A) and longitudinal (B) gray-scale sonograms of the right thyroid, a PTC (arrows) shows inhomogeneous isoechogenicity, a lobulated margin, an ovoid shape, and no calcifications. C and D, In axial nonenhanced (C) and enhanced (D) CT images, a PTC (arrows) has homogeneously low attenuation, a lobulated margin, an ovoid shape, no calcifications, and homogeneous isoenhancement. A follicular variant of PTC in the right lobe and normal thyroid parenchyma was determined in histopathology.

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Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.

J Comput Assist Tomogr • Volume 38, Number 36, November/December 2014

CT Features of PTC

TABLE 2. Frequency Analysis of CT Features of Papillary Thyroid Carcinomas in 120 Patients

TABLE 3. Comparison of US and CT Features of Papillary Thyroid Carcinomas in 106 Patients

CT Features

Items

CT Detection Nonvisualization Visualization Degree of attenuation Low IsoHigh Pattern of attenuation Homogeneous Inhomogeneous Heterogeneous Margin Smooth Irregular Lobulated Shape Ovoid Round Taller-than-wide Calcifications None Rim (eggshell) Nodular Punctate Complete Mixed (punctate + nodular) Degree of enhancement No/scant Decreased IsoIncreased Pattern of enhancement Homogeneous Inhomogeneous Heterogeneous

Margin Smooth Irregular Lobulated Shape Ovoid Round Taller-than-wide Calcification None Microcalcifications (punctate) Rim (eggshell) Nodular Complete Mixed (punctate + nodular)

Data are number of items, with percentage in parentheses.

14 (11.7) 106 (88.3) 94 (88.7) 6 (5.7) 6 (5.7) 99 (93.4) 7 (6.6) 0 (0) 42 (39.6) 45 (42.5) 19 (17.9) 18 (17.0) 33 (31.1) 55 (51.9) 70 (66.0) 1 (0.9) 13 (12.3) 13 (12.3) 6 (5.7) 3 (2.8) 7 (6.6) 78 (73.6) 20 (18.9) 1 (0.9) 86 (81.1) 18 (17.0) 2 (1.9)

US

CT

P 0.559

33 (31.1) 54 (50.9) 19 (16.7)

42 (39.6) 45 (42.5) 19 (17.9)

30 (28.3) 35 (33.0) 41 (38.7)

18 (17.0) 33 (31.1) 55 (51.9)

59 (55.7) 29 (27.4) 5 (4.7) 3 (2.8) 1 (0.9) 9 (8.5)

84 (70) 13 (12.3) 1 (0.9) 13 (12.3) 6 (5.7) 3 (2.8)

0.001

Computed tomography features of papillary thyroid carcinomas.

No previous study has been reported on computed tomography (CT) features of papillary thyroid carcinoma (PTC). This study aimed to evaluate CT feature...
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