Thyroid Ultrasonography: Pitfalls And Techniques

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Pictorial Essay Neuroimaging and Head and SN 1229-6929 · eISSN 2005-8330Korean J Radiol 2014;15(2):267-276Thyroid Ultrasonography: Pitfalls and TechniquesSeon Hyeong Choi, MD1, 2, Eun-Kyung Kim, MD1, Soo Jin Kim, MD1, 3, Jin Young Kwak, MD11Department of Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine, Seoul 120-752, Korea; 2Departmentof Radiology, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul 110-746, Korea; 3Department of Radiology, ChungAng University Hospital, Seoul 156-755, KoreaThyroid ultrasonography (US) plays a key role in the diagnosis and management of thyroid-related diseases. The aim ofthis article was to illustrate various pitfalls that can occur in utilizing thyroid US and techniques to prevent them. In thisarticle, we present cases demonstrating the common pitfalls associated with US equipment, performance, normal thyroidstructures, misinterpretations, and surrounding structures. Knowledge of these areas is essential to avoid misdiagnosis orimproper disease management.Index terms: Thyroid nodule; Thyroid; Ultrasonography; Pitfall; TechniqueINTRODUCTIONUltrasonography (US) plays an important role in thediagnosis and management of thyroid-related diseases. Thedevelopment of high resolution US equipment has greatlyinfluenced the management of thyroid nodules; indeed,currently US is frequently used as a first-line diagnostictool, in both guidance of fine needle aspiration biopsy(FNAB) and for post-operative follow-up imaging. Since1985, there have been numerous reports about thyroid US.However, most reports focus on the information gained fromthe actual imaging itself, such as results from assessment ofReceived December 15, 2012; accepted after revision January 14,2014.Corresponding author: Jin Young Kwak, MD, Department ofRadiology, Research Institute of Radiological Science, YonseiUniversity College of Medicine, 50-1 Yonsei-ro, Seodaemun-gu,Seoul 120-752, Korea. Tel: (822) 2228-7400 Fax: (822) 393-3035 E-mail: docjin@yuhs.acThis is an Open Access article distributed under the terms ofthe Creative Commons Attribution Non-Commercial 3.0) which permitsunrestricted non-commercial use, distribution, and reproduction inany medium, provided the original work is properly cited.kjronline.orgKorean J Radiol 15(2), Mar/Apr 2014the nodule, FNAB, or volumetry (1-10). To our knowledge,there is currently a paucity of articles presenting tips orpitfalls related to utilizing this modality (11, 12).The intent of this pictorial review was to providea framework for sharing interpretative and technicalrecommendations regarding thyroid US. We will detailnormal thyroid and peri-thyroid anatomy, and thenattempt to address common pitfalls associated with USequipment, examination skills, anatomy, interpretation, andextrathyroidal abnormalities (Table 1).Normal AnatomyThe thyroid gland is a butterfly-shaped organ locatedin the midline of the anterior neck. It has two elongatedlateral lobes (right and left), and is connected by theisthmus (Fig. 1). Approximately 40% of individuals havea pyramidal lobe arising from the isthmus that extendstowards the hyoid bone (8, 13); this may be misinterpretedas a mass when it is enlarged (Fig. 2).The length of the lateral lobes is approximately 4–5 cm,with the transverse and antero-posterior diameter of thelateral lobes being approximately 2 cm and the thickness267

Choi et al.Table 1. Pitfalls of Thyroid UltrasonographyPitfalls associated with equipmentProbesEquipment settingPitfalls associated with examination skillsLesion locationMuscle interfaceSatisfactory of search: blind areaPitfalls associated with anatomyPosterior septaVascular structuresTransverse process of vertebraePitfalls associated with isPitfalls associated with extrathyroidal abnormalitiesPharyngoesophageal diverticulumTracheal air cystParathyroid hyperplasia or adenomaof the isthmus being less than 0.5 cm (8, 13, 14). Theparenchymal echogenicity of a normal thyroid gland ishomogeneous and higher than the overlying strap muscles ofthe neck. On a cross-sectional image, common carotid arteriesand the internal jugular veins are typically visualized laterallyadjacent to both thyroid lobes (Fig. 1). The esophagus isusually located to the left of the trachea. The parathyroidglands lie close to the deep surface of the thyroid gland butare generally unseen on US when they are normal. Some levelVI lymph nodes can be seen adjacent to the lower poles.Pitfalls Associated with EquipmentFor proper thyroid examination, a high frequency (10–15MHz, at minimum more than 7.5 MHz) linear transducer isrecommended (8, 15, 16). During thyroid US, transverseand longitudinal images should be obtained, while colorDoppler images may be useful in selective cases (6). TheFig. 1. Normal transverse US of thyroid gland. Cross-sectional US shows normal thyroid glands and surrounding structures. Both thyroidglands show homogeneous parenchymal echogenicity higher than anterior strap muscles. Both CCAs run laterally adjacent to both thyroid lobesand infrahyoid strap muscles overlie thyroid gland. Both SCM muscles are located antero-laterally and longus colli muscles are seen posterolaterally to thyroid gland. US ultrasonography, SCM sternocleidomastoid muscle, CCA common carotid artery, IJV internal jugular vein,Ant. Strap m anterior strap muscle, Longus Colli m longus colli muscleABFig. 2. Pyramidal lobe in 49-year-old woman with hypothyroidism.A. On transverse ultrasonography small isoechoic mass (arrows) was seen at superior aspect of left thyroid lobe. B. Lesion (arrows) had sameechogenicity as surrounding thyroid gland; thus, providing important diagnostic clue on longitudinal view.268Korean J Radiol 15(2), Mar/Apr 2014kjronline.org

Thyroid Ultrasonographyconvex transducer may be used in particular cases such asintrathoracic goiter.Pitfalls Associated with Examination SkillsWhen performing thyroid US, proper compression isABFig. 3. Deep located lesion in left thyroid lobe in 35-year-old man.A. Without compression, ill-defined, taller-than-wide hypoechoic nodule (small arrows) suggesting suspicious nodule is visible. B. Followingcompression, margin of nodule can be seen more easily and carotid artery (large arrows) is also compressed.ABFig. 4. Artifact related with muscle interface in 28-year-old man.A. Before compression, hypoechoic lesion (arrows) is visible in anterior portion of right thyroid lobe. B. Following compression, lesiondisappeared as it was pseudo-lesion caused by shadow (field with dots) from sternocleidomastoid muscle interface.kjronline.orgKorean J Radiol 15(2), Mar/Apr 2014269

Choi et al.essential: insufficient force may lead to imaging artifactsdue to the round, protruding structure of the neck. The firstsuch artifact discovered that can be linked to morphologicchange is caused by inadequate pressure of the probe andit is associated with lesion location (Fig. 3). Failure toapply adequate pressure results in deeper lesions appearingmore indistinct because of ultrasound attenuation. Theattenuation is in proportion to frequency and is mainlycaused by absorption (17). This can be controlled withtime-gain-compensation (TGC) and gentle but properprobing pressure. Thus, the US performer should apply moreforce to the transducer and trim the focusing or TGC curve.The second type of artifact commonly encounteredis posterior shadowing related to muscle interface.The shadowing is associated with sound transmissionand different sound attenuation causes shadowing andenhancement. Unfortunately, artificial acoustic shadowingcan result from the critical angle created by a steeplyobliquely oriented tissue plane but it can be eradicated withfirmer compression (18, 19). Such a shadow, mistakenlydeemed a lesion, is sometimes referred to as a pseudolesion (Fig. 4). In the case of thyroid US, the interfaceABFig. 5. Satisfaction of search in 51-year-old man with benign nodule.CA. Outside ultrasonography showed nodule (arrows) in right thyroid lobe. B, C. However, another suspicious nodule was detected at tip of right upperpole. Lesion in upper pole was surgically confirmed to be papillary carcinoma, but lesion in lower pole was confirmed to be adenomatous hyperplasia.Fig. 6. Blind areas of thyroid gland on ultrasonography. Tips of thyroid gland are easily missed. It is imperative to look for triangularshaped echogenic ends (color drawings) of both poles.270Korean J Radiol 15(2), Mar/Apr 2014kjronline.org

Thyroid Ultrasonographybetween the sternocleidomastoid muscle and infrahyoidmuscles may mimic an ill-defined hypoechoic lesion. Toavoid misdiagnosis, the US performer must compress thetransducer appropriately and confirm lesions on bothtransverse and longitudinal scan views.“Satisfaction of search (SOS)” is a subset of under-readingerrors (false-negative responses) and it occurs when oneor more lesions remain undetected after the detection ofothers (20). In thyroid US, when multiple nodules are seenon US, some nodules might be missed (Fig. 5). Commonlyoverlooked sites are the four tips of the thyroid upperand lower poles. To avoid error, the US technician mustexamine the thyroid gland from tip-to-tip in its entirety,while paying special attention to each tip’s triangular shape(Fig. 6). This is particularly important for novices; using achecklist form is recommended to avoid SOS errors.Pitfalls Associated with AnatomyThere are several normal structures within the neck thatmay influence examination and can potentially mimicpathologic lesions. The first structure of issue is: theechogenic septum within the thyroid gland (Fig. 7). Thisseptum makes a posterior shadow resulting in a posteriordark region that may resemble a hypoechoic lesion. Inpatients with Hashimoto thyroiditis, echogenic septamay be the cause of multiple hypoechoic lesions termedpseudo-nodules (8). When these septa are visualized, it isimperative to turn the transducer and confirm the lesion onboth transverse and longitudinal scans.The second normal structure often mistaken for apathologic lesion is the blood vessel. The thyroid glandis supplied by superior and inferior thyroid arteries anddrains into superior, middle, and inferior thyroid veins. Thesuperior thyroid artery primarily supplies the anterior aspectof the thyroid lobe, while the inferior thyroid artery suppliesthe posterior aspect. In some patients, these vascularstructures mimic a suspicious elongated nodule at theposterior aspect of the thyroid gland (Fig. 8). Occasionally,the inferior thyroid artery or vein appears like a noduleon US (Fig. 9). In these cases, color Doppler images withgraded compression become useful in ruling out vascularFig. 7. Pseudo-lesion caused by posterior thyroid septum. Thyroid lobulation caused by septum (arrows) may be misdiagnosed asparathyroid lesion or thyroid nodule. In this instance, turning probe results in abrupt discontinuation of septum, and provides additionaldiagnostic assistance.ABCFig. 8. Vascular structure mimicking thyroid nodule.A. Irregular, taller-than-wide, hypoechoic lesion (arrows) was seen at posterior aspect of left mid thyroid pole. B. Color Doppler scan revealedvascular structure. C. Vascular structure likely arose from inferior thyroid artery (arrow). Spectral wave form on Doppler scan would help confirmation.kjronline.orgKorean J Radiol 15(2), Mar/Apr 2014271

Choi et al.structures.Finally, the transverse vertebral processes of the cervicalspine or a cervical rib may also present opportunity formisidentification by mimicking calcified jugular chainlymph nodes. These structures show up as echogeniclesions with an intense posterior shadowing on US (Fig.10). This diagnostic dilemma may be particularly importantAin patients who have previously undergone thyroidectomyfor thyroid cancer. According to previous reports (21,22), intranodal calcifications have been noted in 46%to 69% of metastatic lymph nodes from thyroid papillarycarcinoma (Fig. 11). Intranodal calcifications may also beseen in tuberculosis, sarcoidosis, treated lymphoma, andfollowing radiation or chemotherapy (21-23). Thus, the USBCFig. 9. Vascular structure mimicking thyroid nodule.A. Taller-than-wider lesion is visible at left lower thyroid pole. B, C. On color Doppler scan, it was proven to be vascular structure; inferior thyroidvein (arrow).ABFig. 10. Prominent vertebral transverse process mimicking calcified lymph nodes.A. Circle indicates anterior tubercle of transverse process and square identifies posterior tubercle. Echogenic line (arrows) suggested vertebralcortex. B. Sectional diagram provides more detailed explanation.Fig. 11. Dense calcified lymph node mimicking vertebral transverse process. 69-year-old woman was referred to our hospital fordiagnosed thyroid cancer (arrows). During preoperative thyroid ultrasonography, dense calcification (curved arrows) was visible at left level IVregion. It was initially confused with vertebral transverse process, but was finally determined to be metastatic lymph node.272Korean J Radiol 15(2), Mar/Apr 2014kjronline.org

Thyroid Ultrasonographytechnician should be alert to these similarities, and attemptto differentiate the transverse processes from metastaticlymph nodes when evaluating the lateral neck. In thisinstance, however, if the examiner were to perform FNABof the transverse process, normal soft tissue smears wouldresult (24).Pitfalls Associated with InterpretationMyriad criteria have already been established forFig. 12. Typical comet-tail artifact in benign colloid cyst. 58-year-old woman who had undergone mastectomy for breast cancer waspresented for screening thyroid ultrasonography. Small cyst containing echogenic spot with comet-tail (arrows) was identified. This is typicalcase of “comet-tail artifact” caused by colloid crystals.Fig. 13. Subacute thyroiditis. 48-year-old woman was referred for suspicious left thyroid lesion. Ultrasonography revealed irregular hypoechoicmass (arrows) in her left upper pole. Vascularity was noted at some peripheral areas on color Doppler imaging. Patient had experienced neck painwithin past several weeks. Fine needle aspiration biopsy was performed and confirmed subacute thyroiditis.Fig. 14. Focal lymphocytic thyroiditis. 40-year-old woman underwent thyroid US for evaluation of hypothyroidism. Suspicious hypoechoiclesion (arrows) was seen in mid pole of right thyroid lobe. However, lesion was confirmed to be lymphocytic thyroiditis by US-guided fine needleaspiration biopsy. US ultrasonographykjronline.orgKorean J Radiol 15(2), Mar/Apr 2014273

Choi et al.differentiating benign thyroid lesions from malignant lesions(6, 25-29). One of the well-known findings associatedwith thyroid cancer is microcalcification associatedwith psammoma bodies. This proves to be an importantdiagnostic factor because of its high specificity (1, 29, 30).Although microcalcification is often confused with colloidcrystal as both are seen as echogenic dots on US, a followup with US alone is sufficient in an anechoic cyst with thecharacteristic “comet-tail artifact” (Fig. 12) (31).Certain types of thyroiditis may be misdiagnosed asthyroid malignancy: in particular, subacute and chroniclymphocytic thyroiditis. Park et al. (32) reported thepresence of ill-defined hypoechoic lesions without adiscrete round to oval shape as a US finding associated withsubacute thyroiditis and that clinically, subacute thyroiditiswas also associated with painful neck swelling and/orfever (Fig. 13). The thyroiditis tend to show geographicalchanges on different US views unlike true focal massesand some patients may have a recent upper respiratoryinfection history (32). Langer et al. (33) reported that focalthyroiditis is associated with solid hyperechoic nodules withill-defined margins. Some of these nodules are seen as illdefined, irregular, geographically patterned hypo- to markedhypo-echoic lesions with relatively decreased vascularitycompared to surrounding tissues (Fig. 14). These lesionsmay mimic malignancy; thus, further work-up is warranted.However, results of FNAB are typically consistent withbenign lesions such as benign follicular cells being foundwith or without the presence of macrophages.Pitfalls Associated with ExtrathyroidalAbnormalitiesA well-known example of an extrathyroidal lesionFig. 15. Pharyngoesophageal diverticulum. 63-year-old woman was referred for evaluation of left thyroid nodule. High-resolution ultrasonographyrevealed pharyngoesophageal diverticulum (arrows). Small barium collection (curved arrows) suggesting diverticulum was visible on esophagography.Fig. 16. Right paratracheal air cyst in 47-year-old woman. Screening ultrasonography revealed echogenic mass (arrows) suggestive of aircontaining mass in right paratracheal region. Neck CT scan was performed and confirmed presence of right paratracheal air cyst with slit-likecommunicating channel (arrows). P paratracheal air cyst, T trachea274Korean J Radiol 15(2), Mar/Apr 2014kjronline.org

Thyroid UltrasonographyFig. 17. Parathyroid cyst. 47-year-old woman presented with left-sided neck mass. Ultrasonography revealed large cystic mass (arrows) atinferior aspect of left thyroid lobe. Parathyroid hormone level in aspirate was 100.93 pg/mL, while thyroglobulin level was less than 0.1 ng/mL.ABFig. 18. Parathyroid adenoma in 54-year-old woman.A. Thyroid US revealed hypoechoic solid mass at right lower pole region. B. Color Doppler US showed characteristic peripheral vascularity. It wassurgically shown to be parathyroid adenoma. US ultrasonographymasquerading as thyroid pathology is a smallpharyngoesophageal diverticulum. It has the appearanceof a hypoechoic mass with internal echogenic dots on US;thus, it is often misdiagnosed as a suspicious nodule (Fig.15). However, the shape of diverticulum may change byperistalsis during scanning (12). Rarely, a paratracheal aircyst may also mimic a suspicious thyroid lesion. Indeed,it is similar in appearance to a pharyngoesophagealdiverticulum but is usually located near the rightinferoposterior aspect of the thyroid gland with a narrowstalk (Fig. 16) (12, 34). A third structure also commonlyseen is the parathyroid lesion. Although the normalparathyroid gland is not typically seen on US, parathyroidlesions such as hyperplasia, adenomas or cysts may be seennear the posterior or inferior aspect of the thyroid gland(Fig. 17). Typically, the parathyroid adenoma appears as awell-circumscribed, round or oval, hypoechoic nodule. Notfrequently, the parathyroid adenoma may develop cysticdegeneration and contain calcifications (Fig. 18), andkjronline.orgKorean J Radiol 15(2), Mar/Apr 2014if this type of pathology is also present, it may lead tomisdiagnosis (14, 15).CONCLUSIONIn conclusion, the diagnostic performance of thyroidUS can be limited by various imaging pitfalls associatedwith US techniques, performance, and misinterpretation ofnormal structures, or non-thyroidal lesions. A familiarity ofthese pitfalls may help clinicians and patients avoid furtherunnecessary evaluation and misdiagnosis.REFERENCES1. Kim EK, Park CS, Chung WY, Oh KK, Kim DI, Lee JT, et al. Newsonographic criteria for recommending fine-needle aspirationbiopsy of nonpalpable solid nodules of the thyroid. AJR Am JRoentgenol 2002;178:687-6912. Mazzaferri EL. Management of a solitary thyroid nodule. NEngl J Med 1993;328:553-559275

Choi et al.3. Rosen IB, Azadian A, Walfish PG, Salem S, Lansdown E,Bedard YC. Ultrasound-guided fine-needle aspiration biopsy inthe management of thyroid disease. Am J Surg 1993;166:3463494. Yokozawa T, Miyauchi A, Kuma K, Sugawara M. Accurate andsimple method of diagnosing thyroid nodules the modifiedtechnique of ultrasound-guided fine needle aspiration biopsy.Thyroid 1995;5:141-1455. Koike E, Y

A. Outside ultrasonography showed nodule (arrows) in right thyroid lobe. B, C. However, another suspicious nodule was detected at tip of right upper pole. Lesion in upper pole was surgically confirmed to be papillary carcinoma, but lesion in lower pole was confirmed to be adenomatous hyperplasia. Fig. 6. Blind areas of thyroid gland on .

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