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Sonographic Features of Medullary Thyroid Carcinomas According to Tumor Size

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Sonographic Features of Medullary

Thyroid Carcinomas According to

Tumor Size

Comparison With Papillary Thyroid Carcinomas

edullary thyroid carcinoma is a malignant tumor originating from parafollicular C cells of the thyroid, which secrete calcitonin and other neuroendocrine peptides.1

Approxi-mately 75% are sporadic, and 25% are inherited.2 This tumor

accounts for 3% to 4% of all thyroid malignant tumors.3It has a more

aggressive behavior than the well-differentiated thyroid carcinoma, and 10-year mortality rates for patients with medullary thyroid car-Liguang Zhou, MD, Bo Chen, MD, Miaoqing Zhao, MD, Huawei Zhang, MD, Bo Liang, MD

Received June 5, 2014, from the Departments of Ultrasound (L.Z., H.Z., B.L.) and Pathology (M.Z.), Provincial Hospital Affiliated With Shandong University, Jinan, China; and Department of General Surgery, Qilu Hospital of Shandong University, Jinan, China (B.C.). Revision requested July 24, 2014. Revised manu-script accepted for publication September 19, 2014.

This study was supported by the National Natural Science Foundation of China (grant 81102019), the Foundation of Shandong Provincial Science and Technology Development Program (grant 2012G002182), and the Shandong Province Young and Middle-Aged Scientists Research Awards Fund (grant 2012BSBl4065). Liguang Zhou and Bo Chen are co–first authors.

Address correspondence to Bo Liang, MD, Department of Ultrasound, Provincial Hospital Affiliated With Shandong University, 250021 Jinan, China.

E-mail: slyyliangbo@sina.com

M

Objectives—The aim of this study was to evaluate the differences in sonographic features of medullary thyroid carcinomas according to nodule size and compared with findings for papillary thyroid carcinomas.

Methods—This study included 38 medullary thyroid carcinoma nodules and 91 pap-illary thyroid carcinoma nodules, which were confirmed by pathologic examination between May 2008 and September 2013. Nodules were divided into those that were greater than 10 mm (large nodules) and 10 mm or less (small nodules). The differences in sonographic features (composition, echogenicity, margin, calcifications, and shape) between groups were analyzed with a χ2test.

Results—Large medullary thyroid carcinomas more frequently showed an ovoid-to-round shape and a smooth margin; small medullary thyroid carcinomas more frequently showed a taller-than-wide shape and a spiculated margin; the differences were statistically significant between the groups (P< .05). Compared with papillary thyroid carcinomas, large medullary thyroid carcinomas tended to have an ovoid-to-round shape, a smooth margin, and macrocalcifications and were more frequently diagnosed as indeterminate nodules (P< .05); however, there were no significant differences in the internal compo-sition, calcifications, echogenicity, margin, and shape between small medullary thyroid carcinomas and small papillary thyroid carcinomas (P> .05).

Conclusions—Our data indicate that the sonographic features of medullary thyroid car-cinomas are associated with tumor size; furthermore, the sonographic features of medullary thyroid carcinomas are similar to those of small papillary thyroid carcinomas but greatly different from those of large papillary thyroid carcinomas. Large medullary thyroid carcinomas are more commonly diagnosed as indeterminate nodules by sonog-raphy than large papillary thyroid carcinomas, and fine-needle aspiration biopsy or serum calcitonin measurement may be helpful.

Key Words—head and neck ultrasound; medullary thyroid carcinoma; papillary thyroid carcinoma; sonography; thyroid gland

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cinomas vary from 13.5% to 38%.4–6Therefore, early and

precise preoperative diagnosis is fundamental to improve survival rates for patients with this tumor.

Sonography is a useful tool for detecting and diagnos-ing thyroid diseases, especially thyroid nodules. Numerous studies have reported the sonographic appearance of pap-illary thyroid carcinomas, such as the presence of a solid or predominantly solid composition, hypoechogenicity, microcalcifications, an irregular or spiculated margin, and a taller-than-wide shape.7–10However, at present, the

sono-graphic features of medullary thyroid carcinomas remain open, and few studies have analyzed sonographic fea-tures associated with this cancer type,11–14 which is

attrib-uted to its lower prevalence and diversified sonographic features. We speculate that diversified sonographic features might be related to the differential growth stages of the tumor. In this study, we focused on evaluating the sono-graphic features of medullary thyroid carcinomas accord-ing to nodule size and compared them with the sonographic features of papillary thyroid carcinomas to further define the sonographic features of medullary thyroid carcinomas and determine which features are different from those of papillary thyroid carcinomas.

Materials and Methods

Patients

This retrospective study was approved by the Institutional Review Board, and the need for informed consent was waived. From May 2008 to September 2013, a total of 124 consecutive patients received preoperative sonographic examinations and subsequently underwent thyroidectomy for nodular thyroid disease at the Provincial Hospital Affiliated With Shandong University. Among them, 37 patients (38 nodules) had a diagnosis of medullary thyroid carcinoma confirmed by pathologic examination (22 female and 15 male; age range, 20–70 years; mean age ± SD, 47.9 ± 12.4 years), and 87 patients (91 nodules) had a diagnosis of papillary thyroid carcinoma confirmed by pathologic examination (51 female and 36 male; age range, 27–76 years; mean age, 50.4 ± 14.3 years).

Sonographic and Cytologic Examinations

All sonographic examinations were performed with a LOGIQ E9 ultrasound system (GE Healthcare, Milwaukee, WI) a 750 XG ultrasound system (Toshiba Medical Systems Co, Ltd, Tokyo, Japan) equipped with a 10–15-MHz linear array transducer. Examinations were conducted and recorded by 2 skilled sonographers, and findings were prospectively described according to the following

param-eters: size, composition, echogenicity, margin, calcifications, and shape. To match each nodule found at pathologic examination to the corresponding nodule on sonography, we took into account its location; all nodules were included in the study when it was possible to correlate exactly the locations of the nodules on sonography with the patho-logic examination. With respect to the size of the nodules, the largest diameter measured by sonography was selected and was expressed as the mean ± standard deviation, and the nodules were divided into 2 groups: nodules of greater than 10 mm (large nodules) and nodules of 10 mm or less (small nodules). Sonographic features were classified by com-position (solid, >50% solid, or <50% solid), echogenicity (hyperechoic, isoechoic, hypoechoic, or markedly hypo -echoic), margin (smooth, spiculated, or poorly defined), calcifications (microcalcifications or macrocalcifications), and shape (ovoid to round, taller than wide, or irregular). According to Korean Society of Thyroid Radiology 2011 guidelines,15each nodule was identified as suspiciously

malignant, indeterminate, or probably benign. Malignant sonographic features were defined as marked hypo -echogenicity or hypo-echogenicity, microcalcifications and macrocalcifications, a taller than-wide shape, and a spicu-lated margin. Nodules with any of these features were considered suspiciously malignant. A probably benign nodule was defined as a simple cyst, a predominantly cystic or cystic nodule with reverberating artifacts, or a nodule with a spongiform appearance (especially with intervening isoechoic parenchyma). Indeterminate nod-ules were defined as nodnod-ules that did not show any suspi-cious or benign findings.

After the sonographic features were assessed, some of patients underwent a cytologic evaluation, which was per-formed on thyroid nodules with suspicious or indeterminate sonographic features. All fine-needle aspirations were per-formed under sonographic guidance with a freehand tech-nique using a 23-gauge needle connected to a 10-mL syringe, as previously reported.16 To evaluate the cytologic results for the medullary thyroid carcinomas, suspiciously malig-nant nodules were considered true-positive results (fine-needle aspiration–positive group) and the others were considered false-negative results (fine-needle aspiration– negative group).

Statistical Analysis

SPSS version 11.0 software (IBM Corporation, Armonk, NY) was used for statistical analysis. The comparison of mean nodule sizes was performed with a ttest, and the comparison of frequency distributions was performed with a χ2test. P< .05 was considered statistically significant.

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Results

Among 38 medullary thyroid carcinoma nodules, 7 were small nodules, and 31 were large nodules. The mean size of the nodules was 14.2 ± 7.5 mm (range, 6.4–54.6 mm). Among 91 papillary thyroid carcinoma nodules, 23 were small nodules, and 68 were large nodules. The mean size of the nodules was 16.7 ± 9.6 mm (range, 4.3–52.7 mm). The mean size was not statistically different between the medullary and papillary thyroid carcinomas (P> .05).

The sonographic features of large medullary thyroid carcinomas are presented in Table 1 and Figure 1, A–C. Large medullary thyroid carcinomas were solid (96.8%), were markedly hypoechoic (35.5%) or hypoechoic (61.3%), had an ovoid-to-round shape (61.3%), had microcalcifications (22.6%) or macrocalcifications (38.7%), and had a smooth margin (58.1%). Compared with large papillary thyroid carcinomas (Figure 2A), large medullary thyroid carcinomas tended to have an ovoid-to-round shape, a smooth margin, and macrocalcifications (P< .05); the internal composition and echogenicity were equal to those of large papillary thyroid carcinomas (P> .05). Of the 31 large medullary thyroid carcinomas, 20 (64.5%) nodules were classified as suspiciously malignant; 11 (35.5%) were classified as indeterminate, and none was classified as probably benign on sonography. Suspiciously malignant nodules were found less frequently, and indeterminate nodules were found more frequently in large medullary thyroid carcinomas than large papillary thyroid carcinomas (P< .05).

As shown in Table 2 and Figure1D, the predominant sonographic features of small medullary thyroid carcinomas were a solid composition (100%), marked hypo -echogenicity (57.1%) or hypo-echogenicity (42.9%), a spiculated margin (85.7%), microcalcifications (14.7%), and a taller-than-wide shape (57.1%). There were no sig-nificant differences compared with small papillary thyroid carcinomas (Figure 2B; P> .05). For the 7 small medullary thyroid carcinomas, 5 nodules (71.4%) were classified as suspiciously malignant; 2 (27.8%) were classified as inde-terminate; and none was classified as probably benign. There was no statistical difference for the diagnosis of nod-ules between small medullary and small papillary thyroid carcinomas (P>0.05).

A comparison between small and large medullary thy-roid carcinomas is summarized in Table 3. There were no significant differences in the internal composition, micro-calcifications, and echogenicity between the groups (P> .05). However, small nodules showed a taller-than-wide shape and a spiculated margin more frequently, whereas large

nodules were more associated with an ovoid-to-round shape and a smooth margin (P< .05).

Of the 37 patients with medullary thyroid carcinomas, 23 (62.2%) underwent preoperative fine-needle aspiration. On the basis of cytologic results, 10 nodules were true pos-itive (43.5%), and 13 were false negative (56.5%).

Discussion

The advent of high-resolution sonography and its wide-spread use have improved detection of thyroid nodules, with a consequent increase in diagnosis of small tumors.17,18

In this study, we divided nodules into small (≤10 mm) and large (>10 mm) groups. The differences in the sonographic features of medullary thyroid carcinomas between small and large nodules were investigated. To date, only 1 report19

about the sonographic features of medullary thyroid carcinomas according to tumor size has been published, which concluded that medullary thyroid carcinomas smaller than 10 mm tend to have a spiculated margin, and those larger than 10 mm tend to have a smooth margin. Our study yielded similar results, and the differences in shape and

Table 1. Sonographic Features of Medullary and Papillary Thyroid Carcinomas With a Nodule Size of Greater Than 10 mm

Medullary Papillary Carcinoma Carcinoma Sonographic Feature (n = 31) (n = 68) P Diagnosis, n (%) Probably benign 0 0 NA Indeterminate 11 (35.5) 11 (16.2) .032 Suspiciously malignant 20 (64.5) 57 (83.8) .99 Composition, n (%) Solid 30 (96.8) 60 (88.2) .170 >50% solid 1 (3.2) 7 (10.3) .424 <50% solid 0 1 (1.5) >.99 Echogenicity, n (%) Hyperechoic 0 0 Isoechoic 1 (3.2) 9 (13.2) .241 Hypoechoic 19 (61.3) 38 (55.9) .614 Markedly hypoechoic 11 (35.5) 21 (30.9) .650 Shape, n (%) Ovoid to round 19 (61.3) 14 (20.6) <.001 Taller than wide 4 (12.9) 35 (51.5) .001

Irregular 8 (25.8) 19 (27.9) .825 Margins, n (%) Smooth 18 (58.1) 14 (20.6) <.001 Spiculated 7 (22.6) 34 (50.0) <.001 Poorly defined 6 (19.3) 20 (29.4) .292 Calcifications, n (%) Microcalcifications 7 (22.6) 30 (44.1) .040 Macrocalcifications 12 (38.7) 8 (11.8) .002 NA indicates not applicable.

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margins were statistically significant between the groups, with large medullary thyroid carcinomas more frequently showing an ovoid-to-round shape and a smooth margin and small medullary thyroid carcinomas more frequently showing a taller-than-wide shape and a spiculated margin. It was speculated that the difference might be attributable to the differential growth pattern according to tumor size or the possibility of different subsets of medullary thyroid carcinoma with different genetic backgrounds. Thus, our results suggest that different criteria for sonographic diag-nosis of medullary thyroid carcinomas are needed for nod-ules of different sizes.

Several previous studies evaluated sonographic features of medullary thyroid carcinomas compared with papillary thyroid carcinomas. Kim et al11found that an

ovoid-to-round shape was significantly more prevalent for medullary

thyroid carcinomas than papillary thyroid carcinomas, whereas echogenicity, cystic changes, borders, and calcifi-cations were not significantly different between the types. Lee et al14reported that, compared with papillary thyroid

carcinomas, medullary thyroid carcinomas tended to show an oval-to-round shape and a circumscribed margin. To our knowledge, a study investigating the difference between medullary and papillary thyroid carcinomas according to nodule size has not been reported previously. We found that small medullary thyroid carcinomas had no significant difference from small papillary thyroid carcino-mas in internal composition, calcifications, echogenicity, margin, and shape (P> .05), whereas large medullary thyroid carcinomas tended to an ovoid-to-round shape, a smooth margin, and macrocalcifications compared to papillary thyroid carcinomas larger than 10 mm.

Consid-Figure 1. Different sonographic features of medullary thyroid carcinomas. A, Longitudinal sonogram of medullary thyroid carcinoma in a 70-year-old woman showing a solid composition, hypoechogenicity, a smooth margin, an ovoid-to-round shape, and macrocalcifications. B, Longitudinal sono-gram of medullary thyroid carcinoma in a 54-year-old man showing a solid composition, marked hypoechogenicity, a spiculated margin, and an irregular shape. C, Longitudinal sonogram of medullary thyroid carcinoma in a 39-year-old woman showing a solid composition, hypoechogenic-ity, a smooth margin, macrocalcifications, and an ovoid-to-round shape. D, Longitudinal sonogram of medullary thyroid carcinoma (arrow) in a 34-year-old woman (nodule size, 6.4 mm) showing a solid composition, marked hypoechogenicity, a spiculated margin, and a taller-than-wide shape.

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ering an ovoid-to-round shape and a smooth margin, which is not a suspiciously malignant feature, large medullary thyroid carcinomas were more frequently diag-nosed as indeterminate nodules than large papillary thy-roid carcinomas (P< .05). According to Korean Society of Thyroid Radiology guidelines, all nodules with suspi-ciously malignant sonographic features should undergo fine-needle aspiration, whereas only nodules larger than 10 mm should undergo fine-needle aspiration if they are inde-terminate on sonography. Based on the Korean Society of Thyroid Radiology guidelines, small medullary thyroid car-cinoma nodules with indeterminate sonographic features would have not met criteria for fine-needle aspiration. However, if every sonographically indeterminate nodule of any size underwent fine-needle aspiration, the burden would be large. Moreover, fine-needle aspiration has been shown to have low sensitivity for diagnosing medullary thyroid carcinoma.20In our study, the false-negative fine-needle aspiration rate for medullary thyroid carcinoma was 56.5%. Therefore, medullary thyroid carcinomas with indeterminate sonographic features and false-negative fine-needle aspiration results may lead to misdiagnosis and may not be correctly treated. We did not provide data for serum calcitonin, which is not routinely recommended in the guidelines. Due to the imperfect diagnostic accuracy of sonography and the possible false-negative results of cyto-logic examination by fine-needle aspiration, serum calci-tonin determination is suggested for these patients and should aid in the diagnosis of medullary thyroid carcinoma. This suggestion is given on the basis of research21,22that

confirmed that serum calcitonin measurement was a highly sensitive method for diagnosis of medullary thyroid carci-noma. We plan to collect serum calcitonin data and study

the relationship between medullary thyroid carcinoma and calcitonin in further studies.

Previous studies indicated that microcalcifications had high specificity for prediction of thyroid malignancy.23,24

Figure 2. Different sonographic features of papillary thyroid carcinomas. A, Transverse sonogram of papillary thyroid carcinoma in a 48-year-old woman showing a solid composition, hypoechogenicity, a spiculated margin, microcalcifications, and a taller-than-wide shape. B, Longitudinal sonogram of papillary thyroid carcinoma (arrow) in a 34-year-old woman (nodule size, 8.3 mm) showing a solid composition, marked hypo echogenic-ity, a spiculated margin, microcalcifications, and a taller-than-wide shape.

Table 2. Sonographic Features of Medullary and Papillary Thyroid Carcinomas With a Nodule Size of 10 mm or Less

Medullary Papillary Carcinoma Carcinoma Sonographic Feature (n = 7) (n = 23) P Diagnosis, n (%) Probably benign 0 0 NA Indeterminate 2 (28.6) 7 (30.4) >.99 Suspiciously malignant 5 (71.4) 16 (69.6) <.99 Composition, n (%) Solid 7 (100) 23 (100) NA >50% solid 0 0 NA <50% solid 0 0 NA Echogenicity, n (%) Hyperechoic 0 0 NA Isoechoic 0 0 NA Hypoechoic 3 (42.9) 10 (43.5) >.99 Markedly hypoechoic 4 (57.1) 13 (56.5) <.99 Shape, n (%) Ovoid to round 1 (14.3) 1 (4.4) .418 Taller than wide 4 (57.1) 17 (73.9) .640 Irregular 2 (28.6) 5 (21.7) >.99 Margins, n (%) Smooth 0 2 (8.7) >.99 Spiculated 6 (85.7) 18 (78.3) >.99 Poorly defined 1 (14.3) 3 (13.0) >.99 Calcifications, n (%) Microcalcifications 1 (14.3) 3 (13.0) >.99 Macrocalcifications 0 1 (4.3) >.99 NA indicates not applicable.

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Macrocalcifications, although not as specific as micro-calcifications, were also associated with malignancy.25,26

Our results showed that the incidence of microcalcifica-tions or macrocalcificamicrocalcifica-tions had no significant difference between papillary and medullary thyroid carcinomas with nodule sizes of 10 mm or less. Both microcalcifications and macrocalcifications are commonly seen in medullary thy-roid carcinomas larger than 10 mm; although microcalci-fications are more frequently seen in large papillary thyroid carcinomas, macrocalcifications are more frequently seen in large medullary thyroid carcinomas. This finding can be attributed to the different calcification mechanisms: medullary thyroid carcinoma calcifications are caused by amyloid deposits,27and papillary thyroid carcinoma

calci-fications are caused by psammoma bodies.16

This study had limitations. First, the evaluation of cases was retrospective, and there was an unavoidable selection bias, which could have resulted in an artifact cased by a clin-ical practice pattern of more aggressive tissue sampling for nodules with suspicious features. A prospective analysis may provide more information and reduce the selection bias.

Second, because of the low frequency of medullary thyroid carcinomas, fewer cases were included and were further divided into small and large lesions.

In conclusion, our data indicate that the sonographic features of medullary thyroid carcinoma associated with tumor size more frequently include a taller-than-wide shape and a spiculated margin in small nodules and an ovoid-to-round shape and a smooth margin in nodules larger than 10 mm; furthermore, our findings also suggest that sonographic features for discrimination of medullary thyroid carcinoma from papillary thyroid carcinoma are an ovoid-to-round shape, a smooth margin, and the presence of macrocalcifications in large nodules. Large medullary thyroid carcinomas are more frequently diagnosed as indeterminate nodules by sonography than large papillary thyroid carcinomas.

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Table 3. Sonographic Features of Small and Large Medullary Thy-roid Carcinomas Small Large Sonographic Feature (n = 7) (n = 31) P Diagnosis, n (%) Probably benign 0 0 NA Indeterminate 2 (28.6) 11 (35.5) >.99 Suspiciously malignant 5 (71.4) 20 (64.5) >.99 Composition, n (%) Solid 7 (100) 30 (96.8) >.99 >50% solid 0 1 (3.2) >.99 <50% solid 0 0 NA Echogenicity, n (%) Hyperechoic 0 0 NA Isoechoic 0 1 (3.2) >.99 Hypoechoic 3 (42.9) 19 (61.3) .425 Markedly hypoechoic 4 (57.1) 11 (35.5) .401 Shape, n (%) Ovoid to round 0 19 (61.3) .008

Taller than wide 5 (71.4) 4 (12.9) .004 Irregular 2 (28.6) 8 (25.8) >.99 Margins, n (%) Smooth 0 18 (58.0) .009 Spiculated 6 (85.7) 7 (22.6) .004 Poorly defined 1 (14.3) 6 (19.4) >.99 Calcifications, n (%) Microcalcifications 1 (14.3) 7 (22.6) >.99 Macrocalcifications 0 12 (38.7) .074 NA indicates not applicable.

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