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Interventional Radiology Case Conferences Massachusetts General Hospital |
1 All authors: Department of Radiology, Division of Abdominal Imaging and Intervention, Massachusetts General Hospital, 55 Fruit St., White 270, Boston, MA 02114.
Received January 14, 2003;
accepted after revision January 14, 2003.
Address correspondence to P. R. Mueller.
Case History
 Top Case History References |
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Dr. Titton. For which patients should sonography of the thyroid gland be considered?
Dr. Mueller. Sonograms of the thyroid are obtained to detect and characterize either focal or diffuse thyroid disease. Focal thyroid nodules may come to clinical attention because of physical examination findings or, alternatively, as an incidental radiologic finding on a diagnostic test such as chest CT, carotid sonography, whole-body positron emission tomography (PET), or cervical spine MR imaging ordered for an unrelated indication [1]. The primary goal of sonography in the evaluation of focal thyroid lesions is to determine which thyroid lesions have an indeterminate cause or are suggestive of thyroid cancer and therefore warrant thyroid biopsy. The overall likelihood that a given thyroid nodule is malignant is approximately 5% [2, 3].
Patients with thyroid disorders that affect the entire thyroid gland, such as Graves' disease and thyroiditis, usually present clinically with symptoms of hyper- or hypothyroidism, neck tenderness, or alterations in thyroid size. These patients often undergo diagnostic sonography during the initial evaluation to complement thyroid function studies, to evaluate the overall size of the gland, to evaluate the overall vascularity of the gland, and to exclude focal suspicious thyroid abnormalities.
Dr. Titton. The patient underwent thyroid sonography. The sonograms showed a 2-cm mixed solid–cystic nodule with microcalcifications in the lower pole of the left thyroid lobe (Fig. 1A). Which sonographic features of thyroid nodules warrant thyroid biopsy?
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Dr. Gervais. The decision to biopsy is based on multiple factors including patient-specific factors and sonographic findings. Although no single feature is 100% predictive, several sonographic features are known to increase the likelihood of thyroid malignancy. Suspicious findings of a thyroid nodule on sonography include microcalcifications; marked lesion hypoechogenicity relative to surrounding strap muscle; poorly defined, indistinct, or blurred lesion margins; direct invasion of the nodule through the thyroid capsule; central (rather than peripheral) vascularity within the lesion; and a shape greater in anteroposterior dimension than transverse dimension [1, 4]. Micro-calcifications, defined as tiny shadowing or nonshadowing hyperechoic foci, are more predictive of cancer than any other sonographic finding, with a positive predictive value for thyroid carcinoma of up to 70% [4].
The threshold for biopsy of thyroid nodules should be lowered in a patient with a thyroid nodule who also has risk factors for thyroid cancer. Risk factors of thyroid carcinoma include family history of thyroid cancer and a history of head and neck radiation. In addition, men, individuals younger than 30 years or older than 60 years, and patients with multiple endocrine neoplasia type 2 are at high risk.
A thyroid biopsy may also be requested for a patient with clinical symptoms of a diffuse thyroid abnormality and borderline findings on thyroid function studies to confirm or refute a specific diagnosis. Because diffuse thyroid disease without a focal nodular appearance, architectural distortion, or micro-calcifications is almost invariably benign, a biopsy is usually not warranted in most cases of diffuse thyroid disease.
Dr. Titton. What is the importance of the size of a thyroid nodule?
Dr. Maher. Size is not a reliable indicator of a benign or malignant nature of a thyroid lesion. Suspicious lesions as small as 2 mm have been shown to be both primary thyroid cancers and recurrences in the thyroidectomy bed [5]. In a prospective study by Kim et al. [4], no statistically significant difference between benign and malignant nodules was found with regard to size in 155 nonpalpable thyroid nodules that later underwent fine-needle aspiration.
Diagnosis of small thyroid carcinomas is critical because thyroid carcinomas smaller than 1 cm may be early lymph node metastasis or extranodal invasion [4]. Small nodules (< 1 cm) are undoubtedly more difficult to biopsy, and the diagnostic yield may be lower than for larger nodules. Unless a definitive benign diagnosis is rendered by the pathologist, all suspicious nodules—regardless of size—require ongoing follow-up by the endocrinologist, surgeon, or both. Further management is likely to involve follow-up sonography and may involve a repeated thyroid biopsy.
Dr. Titton. Do findings on nuclear medicine examinations influence the decision about whether to perform thyroid biopsy?
Dr. Boland. Patients with abnormal results on thyroid scintigraphy are always referred directly to the interventional radiology service for sonographically guided thyroid biopsy. In the past, patients were often referred for biopsy of "cold nodules," which are found to be malignant in up to 28% of the cases [6, 7]. The major limitation of thyroid scintigraphy is spatial resolution; even with pinhole collimators, nodules smaller than 1 cm are often difficult to differentiate or impossible to adequately visualize. More recently, many patients have been referred at our institution for thyroid biopsy on the basis of focal abnormal hypermetabolic activity within the thyroid gland after whole-body PET. The major limitation in evaluating the thyroid gland on PET is that physiologic uptake of FDG within the thyroid gland may be moderate or even strikingly intense, and this uptake can easily be mistaken for a thyroid lesion [8].
At our institution, we require that patients who are referred for thyroid biopsy because of abnormal results on nuclear medicine studies undergo sonography before a biopsy is scheduled. Sonography is performed in this setting to overcome the limitations of spatial resolution and the overlap of physiologic and abnormal activity that are inherent to nuclear medicine studies. This practice allows the radiologist to optimize preprocedural planning.
Dr. Titton. Are thyroid cancers always solid-appearing on sonography?
Dr. Maher. Many thyroid nodules are complex, exhibiting both cystic and solid components. These nodules can be malignant in up to 15% of cases because any histologic subtype of thyroid cancer may undergo cystic change [9]. As with the evaluation of solid thyroid nodules, size is not a predictor of the underlying histology in cystic thyroid lesions. Cystic lesions should be viewed with concern, particularly in patients with risk factors of thyroid cancer; in patients with manifestations of invasiveness such as hoarseness, obstruction, and lymphadenopathy; and in patients with a residual mass or cyst recurrence after aspiration [9].
Metastatic lymph nodes in the thyroid bed from papillary carcinoma of the thyroid may also appear complex cystic, or rarely even purely cystic, and may present as the initial manifestation of papillary carcinoma of the thyroid in up to 15% of cases [10]. If not suspected by the radiologist, solitary cystic lymph node metastasis may be misinterpreted as a benign cervical cystic mass, and this misinterpretation can delay the correct diagnosis of an occult thyroid carcinoma.
Dr. Titton. When is sonographic guidance necessary in performing biopsies of thyroid nodules?
Dr. Mueller. In most institutions, biopsies of palpable masses are usually performed without sonographic guidance because of the convenience of performing the biopsy in the clinician's office and the decreased overall cost [11]. In our practice, sonographically guided fine-needle aspiration is most commonly performed either if a patient has a nonpalpable nodule or multiple thyroid nodules that cannot be differentiated by palpation or if the result of the fine-needle aspiration obtained without imaging guidance is unsatisfactory.
Findings at sonography and at physical examination are not always concordant. In a study directly comparing palpation and high-resolution sonography of the thyroid in 2441 Chernobyl patients, high-resolution sonography failed to confirm the existence of 68% of the nodules found on physical examination. The same study reported that only 21% of the nodules found on sonography of the thyroid were detected on physical examination [12].
In a retrospective study directly comparing sonographically guided fine-needle aspiration biopsy and fine-needle aspiration biopsy guided by manual palpation, researchers found that the accuracy of sonographically guided fine-needle aspiration biopsy was significantly higher than manually guided biopsy (68% vs 48%), particularly for tumors smaller than 2 cm [13]. The conclusion of the study was that sonographically guided fine-needle aspiration biopsy was more likely to achieve a correct diagnosis and avoid unnecessary operations than thyroid biopsy guided by manual palpation.
These study findings were confirmed by Yokozawa et al. [14]. In this study, 678 patients initially diagnosed with benign nodules using manually guided fine-needle aspiration biopsy were reexamined with sonographically guided fine-needle aspiration biopsy. Of the patients initially diagnosed as having benign thyroid nodules, 15% were proven to have a thyroid carcinoma after repeated thyroid biopsy using sonography guidance [14].
Sonographically guided fine-needle aspiration biopsy of the thyroid provides a higher rate of diagnostic accuracy because the needle can be visualized continuously during insertion and lesion sampling and because various portions of the nodule can be sampled. Sonographic guidance is particularly useful in sampling lesions found in firm, lobulated thyroid glands and in sampling lesions that are smaller than 2 cm, which are not always easily palpable [13, 14].
Dr. Titton. How is a sonographically guided biopsy of the thyroid performed?
Dr. Gervais. After we obtain informed written consent from the patient, we ask the patient to lie supine on a stretcher. We place a rolled towel behind the patient's lower cervical spine to aid the patient in extending the neck as much as possible. Sonography is then performed with a high-frequency (7–13 MHz) linear transducer to localize the nodule to be sampled. Once a clear path to the thyroid nodule is identified, the skin overlying the neck is cleansed with betadine. A sterile drape is then placed over the neck, and the sonography probe is covered with a sterile drape. Sterile ultrasound gel is placed on the patient's neck to aid transmission of the ultrasound beam. The operator sits at the patient's head, facing the sonography monitor. The skin and subcutaneous tissues in the projected needle path are then anesthetized using 1% lidocaine (Xylocaine, Astra, Westborough, MA). A 25-gauge needle (Monoject, Sherwood Medical, St. Louis, MO) is then placed into the nodule using continuous sonographic guidance (Fig. 1B).
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Specimens can be obtained either with a nonaspiration capillary-action technique or with a suction aspiration technique. For the nonaspiration capillary-action technique, the needle is vigorously manipulated in a to-and-fro motion through the nodule until a small amount of cellular material is seen in the well of the needle. For the suction aspiration technique, a 10-mL syringe is applied to the hub of the 25-gauge needle, and a similar to-and-fro manipulation of the needle is performed with minimal suction (1–2 mL) to attempt successful aspiration of a cellular specimen. The choice between a nonaspiration and an aspiration technique is a matter of operator preference. Various comparative studies of fine-needle aspiration biopsy without and with aspiration have shown that there is no statistically significant difference between the techniques in diagnostic accuracy [15], so capillary sampling and aspiration techniques should be used in a complementary fashion to obtain diagnostic specimens.
Our most common practice is to start with the nonaspiration capillary-action technique and to switch to the suction aspiration technique only if the initial biopsy passes do not yield cellular specimens. After a biopsy pass, the needle is withdrawn from the neck and the sample is smeared onto glass slides. The slides are then fixed in 95% ethyl alcohol. At our institution, we generally perform from four to six sonographically guided passes into the nodule. Biopsy results are available through the referring physician in approximately 7 days, and patients are instructed to follow up accordingly.
Dr. Titton. What considerations should be kept in mind in order to optimize diagnostic sampling rates?
Dr. Mueller. The radiologist should evaluate the macroscopic appearance of the smear on the glass slide [15]. If any of the smears during the thyroid biopsy appear scant, performing additional passes (up to eight passes) into a nodule should be considered. Samples of different portions of the nodule should be obtained using slightly different needle path trajectories to assess all portions of the nodule. If a nodule has cystic components, the solid cellular component of the nodule should be biopsied to optimize the cellularity of the specimen. The fluid component of the nodule can also be aspirated and sent for cytologic analysis after centrifugation.
Dr. Titton. Does the size of the needle used for performing the thyroid biopsy affect the diagnostic accuracy of the specimens?
Dr. Gervais. In a prospective study, no significant difference was found in diagnostic yield when comparing cellular specimens obtained with 23- and 27-gauge needles [16]. In a separate prospective study directly comparing the fine-needle aspiration biopsy with spring-activated short-throw 18- to 20-gauge core needle biopsy, the diagnostic yield of core biopsy of thyroid nodules exceeded that of fine-needle aspiration techniques by approximately 10% [17]. Core biopsies provided a larger histologic core of tissue, which may affect surgical decision making more than cytologic diagnosis. The drawbacks of core biopsy are that it is a more technically challenging procedure, particularly in lesions smaller than 1.5 cm, and that it has a higher overall complication rate than fine-needle aspiration [18]. For these reasons, core biopsy is considered only in patients with grossly scant-appearing cellular specimens after six to eight fine-needle aspiration passes or in patients who return for repeated biopsy of previously nondiagnostic nodules.
Dr. Titton. When the patient arrived for her scheduled thyroid biopsy, she stated that she was extremely anxious. What measures can be taken in anxious patients to optimize patient cooperation during a thyroid biopsy?
Dr. Boland. When a patient appears especially anxious, the radiologist can significantly affect the patient's perceived overall biopsy experience. The consent process provides an opportunity to answer the patient's questions and to address issues contributing to the patient's anxiety. The extremely low rate of complications (< 1%) of the procedure should be stressed to the patient. During the procedure, many patients become uncomfortable when their face is covered by the sterile drape, reporting sensations of claustrophobia and even difficulty breathing. For this reason, we cover as little of the face as is necessary to maintain a sterile field.
When the biopsy is being performed, the patient should be informed when the subcutaneous lidocaine anesthesia is going to be administered. The patient should also be told to refrain from talking, coughing, or swallowing during the actual needle pass. Between needle passes, the patient should be given an opportunity to clear the throat, cough, and so on to allow the patient some sense of control, thereby minimizing anxiety.
Dr. Titton. Should an on-site cytologist be present during the procedure?
Dr. Mueller. In a prospective study, we compared a group of patients in whom thyroid biopsies were performed without immediate cytologic analysis (four needle passes per lesion) with a group of patients in whom thyroid biopsies were performed with immediate on-site cytologic rapid analysis [19]. In that study, we found no statistically significant difference in cytologic adequacy between the two patient groups. The average procedure time was 12.5 min for the group that underwent biopsy without a cytologist present and was 44.4 min for the group that underwent biopsy with intraprocedural cytologic evaluation [19]. If preprocedural planning is good and intraprocedural technique is optimal, diagnostic specimens are usually obtained—even without a cytopathologist present at the time of the procedure.
Dr. Titton. What is the expected diagnostic yield of sonographically guided fine-needle aspiration biopsy of the thyroid?
Dr. Boland. Reported rates of diagnostic accuracy range from 80% to 95% [2, 15, 17, 20–22]. Lower success rates have been reported for biopsy of cystic thyroid nodules: approximately 30% yield unsatisfactory cytologic results after sonographically guided fine-needle aspiration [19]. In a retrospective study evaluating 178 nondiagnostic sonographically guided fine-needle aspirations, the cystic content of each nodule was the only significant independent predictor of nondiagnostic findings at cytology [22].
Initially nondiagnostic findings for thyroid biopsies should not be considered benign. Follow-up of nodules with initial unsatisfactory biopsy results is up to the discretion of the referring physician, because further management might include repeated biopsy, surgery, or close imaging surveillance. Approximately 10% of excised nodules that had initially nondiagnostic aspirates were found to be malignant [19, 22].
Dr. Titton. Three days after the biopsy, the cytologic findings were positive for papillary carcinoma of the thyroid. What are the limitations of cytologic evaluation?
Dr. Maher. Biopsy specimens that yield only macrofollicular cells or thyroid colloid alone warrant no further investigation and are definitively benign. Similarly, biopsy specimens that yield suspicious, atypical cells with large nuclei or malignant cells require no further diagnostic investigation. Patients with these cytologic findings should undergo surgical excision.
A major problem with cytologic interpretation of fine-needle aspirates is the differentiation of benign Hürthle cells or follicular cell neoplasms from their malignant counterparts [13]. For malignancy to be excluded, lesions that have Hürthle cells at cytologic evaluation are usually surgically excised [23]. Hürthle cells are distinctively large thyroid follicular cells that may be associated with both nonneoplastic conditions of the thyroid, such as Hashimoto's thyroiditis and goiter, or, alternatively, may be associated with thyroid neoplasms.
Furthermore, cytology cannot distinguish between benign microfollicular adenoma and follicular thyroid carcinoma. There is a low but finite probability that a lesion with microfollicular cells after cytologic sampling is a well-differentiated follicular thyroid carcinoma. Differentiation between microfollicular adenomas and follicular carcinomas pathologically is based on the presence or absence of vascular or capsular invasion. For the integrity of the capsule of the lesion to be evaluated, the lesion itself needs to be excised. Approximately 5% of Hürthle cell lesions and 5% of microfollicular lesions prove to be follicular thyroid carcinomas after surgical excision [24].
Dr. Titton. The patient underwent total thyroidectomy, which revealed a multifocal papillary carcinoma of the thyroid. After thyroidectomy the patient was treated with iodine-131 followed by thyroxine therapy. Six months after undergoing thyroidectomy, the patient was diagnosed with a new 8-mm hypoechoic nodule in the thyroidectomy bed (Fig. 1C). What is the utility of sonography in evaluation of the thyroidectomy bed after thyroidectomy, and what are potential pitfalls?
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Dr. Gervais. In general, patients younger than 40 years who have small papillary carcinomas (< 1.5 cm) or minimally invasive follicular carcinomas have the best prognosis after appropriate therapy [24]. Tumor recurrence in the thyroidectomy bed occurs in up to 20% of patients after thyroidectomy [25, 26] and is associated with significant morbidity and even mortality. In a prospective study by Frilling et al. [25], sonography and sonographically guided fine-needle aspiration were found to be more sensitive in the detection of local tumor recurrence (95.3%) than FDG PET, 131I whole-body scintigraphy, and thyroglobulin measurements. Sonographically, the normal postoperative neck shows an absence of thyroid tissue, close apposition of the carotid artery to the trachea, and a group of highly reflective echoes in the thyroidectomy bed that probably represent postoperative scarring [26].
Nodules in the thyroidectomy bed should be considered suspicious and should be biopsied if they increase in size; have microcalcifications; show irregular, intranodular blood flow on color Doppler sonography; or are larger in anteroposterior than transverse diameter.
When the thyroidectomy bed is being assessed on sonography, hypoechoic muscles and normal parathyroid glands should not be mistaken for nodules. Benign lymph nodes and suture granulomas can sonographically mimic tumor recurrence but are often present on the sonograms that are obtained immediately after thyroidectomy. For the assessment of the thyroidectomy bed, review of serial studies and comparison of recent studies with prior studies are essential to evaluate for interval change.
Dr. Titton. In conclusion, can you summarize the usefulness and potential pitfalls of thyroid biopsy?
Dr. Mueller. Thyroid nodules are a common finding and may present either as a clinically palpable finding or as an entirely incidental finding on an imaging examination performed for other indications. Sonography is an extremely useful tool with which to diagnose nodules and to assess features that increase the likelihood that a given nodule may be malignant. Fine-needle aspiration of thyroid nodules is useful in limiting the overall number of patients who require surgery by increasing the number of malignant specimens found at biopsy.
Sonographically guided fine-needle aspiration has been reported to yield higher diagnostic accuracy than fine-needle aspiration alone, even in clinically palpable nodules [13, 14]. The 25-gauge needles are generally sufficient to yield adequate cytologic specimens; however, in selected cases, core biopsy with an 18- to 20-gauge needle may be helpful. Sonographically guided fine-needle aspiration using the nonaspiration-capillary action technique, suction aspiration technique, or both generally yields a diagnostic accuracy of greater than 80%. Cytologic results guide further patient management because patients with noncancerous and nonindeterminate results can be followed up safely [24], and patients with suspicious or malignant results undergo surgical excision. Typically, indeterminate cytologic results that yield microfollicular or Hürthle cells also require surgical excision.
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