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1
Department of Radiology, University of Vienna, Waehringer Guertel 18-20,
A-1030 Vienna, Austria.
2
Department of Radiology, Massachusetts General Hospital, Harvard Medical
School, 55 Fruit St., Boston, MA 02114.
3
Thyroid Unit and Department of Medicine, Massachusetts General Hospital,
Harvard Medical School, Boston, MA 02114.
Received May 30, 2001;
accepted after revision July 30, 2001.
P. Wunderbaldinger was supported by the
Erwin-Schrödinger-Auslandsstipendium of the
Austrian Science Fund, Vienna, Austria.
Abstract
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MATERIALS AND METHODS. Sonographic examinations of 74 patients (47 women, 27 men; mean age, 49 years) with 97 histologically confirmed cystic lymph nodes metastases from papillary thyroid carcinoma were included in the study. The anatomic relationship of the nodes relative to the primary tumor was recorded, and all cystic nodes were qualitatively categorized as either simple (purely cystic) or complex (thickened outer wall, internal nodules, internal septations, and calcifications). All imaging findings were compared with gross pathologic specimens.
RESULTS. Most of the cystic metastases were ipsilateral to the primary tumor (87.8%) and located in the mid or lower jugular chain (73.2%). In 14.9% of all patients, cystic lymph node metastases were the initial manifestation of disease. Only 6.2% of all lymph node metastases were purely cystic (all of these occurred in patients less than 35 years old). Of the 91 complex metastases, a thickened outer wall was present in 35.2% of patients, internal nodules in 42.9%, and internal septations in 57.1%. No calcifications were seen in the 91 complex metastases, and two or more findings were seen in 23.1%. All sonographic findings were verified by surgery.
CONCLUSION. In most of the patients, cystic lymph node metastases are characterized sonographically by the presence of a thickened outer wall, internal echoes, internal nodularity, and septations. However, in younger patients, the lymph nodes might appear purely cystic, thereby mimicking branchial cysts and thus requiring biopsy for final diagnosis and therapy planning.
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Sonography is the imaging method of choice for detecting and characterizing palpable cervical masses, thyroid gland disease, and cervical lymphadenopathy in patients with head and neck cancer [1, 5, 8, 9]. Nodal metastases of papillary carcinomas can appear either as solid or cystic masses. Although solid metastases normally do not represent a diagnostic problem, solitary cystic lymph node metastases might be misinterpreted as a benign cervical cystic mass and therefore could delay the correct diagnosis with the need for more radical treatment [1, 3, 5, 6, 8,9,10].
The aim of our investigation was to illustrate and discuss the sonographic spectrum of surgically proven cystic nodal metastases from papillary thyroid carcinoma with pathologic correlation. Sonographic findings that facilitate the differential diagnosis of these cystic nodal metastases from benign cystic neck lesions will be discussed.
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During clinical workup, all 74 patients underwent a sonographic examination of the neck and a subsequent fine-needle aspiration biopsy of their metastases for histologic confirmation.
Gray-scale sonography was performed using a LogiQ 700 sonography system with a linear 10-MHz transducer (General Electric Medical Systems, Milwaukee, WI) in 38 (51.4%) of 74 patients, using a Diasonics Gateway 2D sonography system with a linear 10-MHz linear transducer (Diasonics Ultrasound, San Jose, CA) in five (7%) of 74 patients, and using an HDI UM 9 sonography system with a linear broadband 10- to 15-MHz transducer (Advanced Technology Laboratories, Seattle, WA) in 31 (42%) of 74 patients. The same standardized machine settings for small parts regions were used for all examinations. Hardcopies of all examinations were printed and analyzed independently by two reviewers who were experienced in head and neck radiology. In case of a differing result, the examination was reread together by both reviewers, and a consensus decision was obtained. The anatomic relationship of the nodes relative to the primary tumor was recorded, and all cystic degenerated lymph nodes were qualitatively categorized as either simple (homogeneously echo free and thin walled) or sonographically complex (presence of a thickened outer wall, internal nodules, internal septations, and calcifications). All imaging findings were compared with gross pathohistologic specimens.
A sonographically guided fine-needle aspiration biopsy using a 25-gauge beveled biopsy needle attached to a syringe was performed in all patients for each lesion. Details of fine-needle aspiration biopsy and specimen handling have been previously described [11]. A mean of three aspirates (range, 2-6) was obtained from each node.
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In 11 patients (14.9%), these cystic lymph node metastases were the initial manifestation of the disease. The diagnosis of cystic lymph node metastases was suspected in only three of these 11 patients on the basis of sonographic findings alone, whereas in the remaining eight patients, the cystic lymph node metastases were initially mistaken for benign cystic neck lesions. In all 11 patients, the final diagnosis of cystic lymph node metastases was made after fine-needle aspiration biopsy.
The lymph nodes were ipsilateral to the primary tumor in 65 (87.8%) of 74 patients and bilateral in nine patients (12.2%). Lymph nodes ranged in size from 1.0 to 3.1 cm (mean, 1.4 cm) in long axis and from 0.5 to 2.8 cm (mean, 1.2 cm) in short axis, as calculated by sonography.
Most of the lymph nodes (71 [73.2%] of 97) were located either in the mid or lower jugular chain, 11 (11.3%) of 97 along the carotid bifurcation, eight (8.2%) in the high jugular chain, and seven (7.2%) in the supraclavicular region.
Only six (6.2%) of the 97 nodes were purely cystic (Fig. 1). Of the 91 complex cystic lymph nodes (93.8% of 97 lymph nodes), a thick outer wall (Fig. 2) was present in 32 (35.2%), internal nodules (Fig. 3A,3B) in 39 (42.9%), and internal septations (Fig. 4A,4B) in 52 (57.1%). Two or more findings were seen in 21 (23.1%) of 91 complex cystic metastases. None of the complex cystic lymph nodes revealed calcifications. All of the sonographic findings were verified by surgery, and the frequency of the assessed findings was not changed by histology.
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No complications occurred during and after fine-needle aspiration biopsy, and the procedure harvested sufficient material for pathologic workup in all 74 patients.
The aspirated fluid was dark and viscous in 62 cases (63.9%), bloody embodied in 21 (21.6%), and yellowish clear in 14 (14.4%). Malignant cells were found by cytology in 71 cases (73.2%), whereas the cytologic profile of the remaining 26 cases (26.8%) did not show any sign of malignancy. (All of these patients had a sonographically visible thyroid tumor suspicious of malignancy.)
Thyroglobulin levels in the aspirated fluid were higher than 40 ng/mL (serum-level cut off) in 78 cases (80.4%). The aspirated fluid in all 78 cases was either dark and viscous or bloody embodied.
After fine-needle aspiration biopsy, all 74 patients underwent surgery; 32 (43.2%) of 74 patients underwent partial thyroidectomy and 42 (56.8%) underwent a complete thyroidectomy. Based on the individual tumor staging, a partial neck dissection was performed in 56 (75.7%) of 74 patients, and the remaining 18 (24.3%) of 74 patients underwent a radical neck dissection. In 26 (35.1%) of 74 patients, adjunct radiotherapy was performed.
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Multiple cystic metastatic nodes or solid lymph node metastases are easy to differentiate from benign cervical cysts such as branchial cleft cysts. However, especially when the lymph nodes are solitary and purely cystic, this distinction might be more difficult. In our series, only 6% of all metastatic nodes were purely cystic on sonography, and all of these were found in patients less than 35 years old, whereas complex cystic metastases were seen only twice in that age group. Therefore, our results are consistent with previous reports in the literature stating that complete cystic degeneration of nodes predominately occurs in young adults, and that the detection of a cystic mass in the neck should alert the physician of an occult thyroid carcinoma [5, 8, 9, 12]. As an explanation for this predomination, it has been advocated that tumors in younger patients tend to be more aggressive, causing extensive liquefaction necrosis and colloid production [4, 8, 12].
As in other series, most of our cystic lymph node metastases were of a sonographic complex nature facilitating the distinction from noninfected branchial cysts [3, 5, 8,9,10]. The main sonographic features for a distinction from noninfected branchial cysts include the following in decreasing order of frequency in our series: internal septations, internal nodules, and a thick outer wall. These sonographic features have been reported to be found rarely in noninfected branchial cysts (reported range, 0-3%) [4, 5, 8,9,10]. Histologically, the internal septations were either caused by solid, papillary structures on fibrovascular stalks, by connective tissue filaments, or by the remaining streaks of lymphoid tissue (residual after the liquefaction necrosis or accompanying intranodal hemorrhage). The papillary structures on fibrovascular stalks are especially known to be typical for papillary thyroid carcinomas and are associated with psammoma bodies and paucity of colloid in the primary tumors [3, 4]. The sonographic visible internal nodules were either caused by partly organized colloid or thyroid tumor cells forming follicles with subsequent colloid production, by (partly) organized intranodal hemorrhage and debris, or by clusters of remaining lymphoid tissue surrounded by carcinomateous elements. Others reported these histologic findings as explanations for the pseudocystic appearance of some of the lymph node metastases derived from papillary thyroid carcinomas [3, 9, 12]. The most unspecific sonographic finding was the thickened wall that was either caused by debris or reactive inflammation or by a combination of the previously mentioned mechanisms.
It has further been advocated that punctuate calcifications are a typical finding of papillary thyroid carcinoma metastases that might help distinguish them from other cystic neck lesions [1, 3, 6, 10]. In our experience, none of the 97 metastases had any form of calcification.
Although being easily distinguishable from noninfected branchial cysts, solitary complex structured cystic metastases may resemble infected and hemorrhagic branchial cysts (Fig. 5A,5B). These complicated brachial cysts are also characterized by an irregular thickened wall, intracystic debris and hemorrhage, and intracystic septations [5, 10]. Because of this resemblance in sonographic appearance, metastatic nodes cannot be accurately differentiated from an infected or hemorraghic branchial cyst, necessitating a more invasive diagnostic approach such as fine-needle aspiration biopsy. Although the general use of fine-needle aspiration biopsy as a diagnostic tool for cystic lesions is somewhat controversial, it has been shown to be useful in almost all cases in which a solid component is noted [8, 9, 11]. In our experience, dark viscous fluid with clearly elevated thyroglobulin concentration was commonly found in the fine-needle aspiration biopsy samples (elevated thyroglobulin in 78 cases [80.4%]; 62 of these cases were dark and viscous) even when typical papillary thyroid carcinoma cells were not. This observation supports the conclusions of Som et al. [3] and King et al. [1] who hypothesized that high intranodal concentration of thyroglobulin reflect areas of high attenuation on CT and inhomogeneous intracystic signal changes on MR imaging, respectively. Therefore, the fluid from these cystic nodes should be sent for thyroglobulin analysis whenever an unclear cystic mass in the neck is present or when the diagnosis of such a mass is in question. The extremely high thyroglobulin concentrations are not really surprising because high fluid thyroglobulin concentrations have been reported to be diagnostic of well-differentiated thyroid carcinoma [4, 11]. On the other hand, clinically, frequent nodal recurrences are found in these patients, but the prognosis appears to be similar to that of typical papillary carcinoma (personal observations, Daniels GH).
Another way to differentiate cystic nodal metastases from benign cystic neck lesions is to identify the primary thyroid tumor. If a primary thyroid tumor is found, most physicians tend to address any cystic cervical lesion and lymph node with more care and as potentially malignant. Whereas in young patients with no visible primary tumor, any cervical cystic lesion is more likely to be addressed as a benign entity such as branchial cleft cyst [1, 3, 5, 6, 12]. Based on our experience, any cystic mass in the mid or lower jugular chain should alert the sonographer to the possibility of thyroid metastases, even in the absence of a demonstrable suspicious thyroid lesion, and thus requires invasive diagnosis.
The major limitations of our study are due to its retrospective design resulting in heterogeneous documentation in some patients. Because of this reason and the absence of the dynamic aspect of the sonographic examination during the evaluation, some of the features of cystic metastases might have been underestimated or missed. Our results might have been further biased by the used patient collective because only patients who underwent thyroid sonography had been included in the study. However, the mere description of sonographic findings in the reported 97 metastases remains unchanged, and all cystic lymph node metastases and all imaging features were verified by surgery and correlated to pathology and histology, thus resulting in a representative sample of disease. Because sonography is still considered the imaging modality of choice for detecting and assessing thyroid gland lesions and cervical lymphadenopathy, the lack of CT and MR imaging, although having been reported to be accurate and useful, does not really influence our study [1, 3, 5, 6, 9, 12].
In conclusion, cystic lymph node metastases may occur in papillary thyroid carcinoma and are characterized sonographically by the presence of a thickened outer wall, internal echoes, internal nodularity, and internal septations in most of the patients. However, especially in younger patients, the lymph nodes might appear as purely cystic masses mimicking branchial cleft cysts. The presence of a solitary asymptomatic lateral cystic mass, especially with a complex sonographic texture, should alert the sonographer to the possibility of a metastases from an occult thyroid carcinoma pending the subsequent assessment of the thyroid gland. In case of an occult primary carcinoma or in case of doubt, one should always verify cystic neck lesions with fine-needle aspiration biopsy.
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