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DOI:10.2214/AJR.07.3443
AJR 2008; 191:598-603
© American Roentgen Ray Society

Original Research

Thyroid Incidentalomas Identified by 18F-FDG PET: Sonographic Correlation

Jin Young Kwak1, Eun-Kyung Kim1, Mijin Yun2, Arthur Cho2, Min Jung Kim1, Eun Ju Son1 and Ki Keun Oh1

1 Department of Radiology, Research Institute of Radiological Science, Yonsei University College of Medicine, 250 Seongsanno (134 Sinchon-dong), Seodaemun-gu, Seoul 120-752, Korea.
2 Division of Nuclear Medicine, Yonsei University College of Medicine, Seoul, Korea.

Received November 18, 2007; accepted after revision February 4, 2008.

 
Supported by a faculty research grant (No. 2006-0152) of Yonsei University College of Medicine for 2006.

Address correspondence to E. K. Kim (ekkim{at}yuhs.ac).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to evaluate the risk of malignancy of thyroid incidentalomas detected on 18F-FDG PET and the diagnostic accuracy of sonography for differentiating benign from malignant focal thyroid incidentalomas that were detected on FDG PET.

MATERIALS AND METHODS. Retrospective review was performed of a database of 87 focal thyroid lesions seen on FDG PET and sonography. Forty-two focal lesions were malignant. We compared the accuracy of the maximum standard uptake value (SUV) to differentiate benign from malignant thyroid lesions. We classified the thyroid nodules as probably benign or suspicious for malignancy by the sonographic features. Statistical analyses compared two subgroups by sonographic classifications between benign and malignant thyroid lesions.

RESULTS. The maximum SUV of the malignant nodules was not significantly higher than that of benign lesions. Thirty-seven (75.5%) of 49 lesions with suspicious sonographic findings revealed malignancy on cytopathology, compared with five (13.2%) of 38 lesions that showed probably benign sonographic findings. These differences were statistically significant using a kappa test ({kappa} = 0.675, p = 0.001) and logistic regression (odds ratio = 26.2, p = 0.001).

CONCLUSION. The probability (48.3%) of malignancy of focal thyroid incidentalomas seen on FDG PET is high. The maximum SUV of thyroid cancer is not significantly higher than that of benign lesions. The probability (13.2%) of malignancy is much lower when the sonographic findings appear benign, as compared with a significantly higher probability (75.5%) of malignancy when the sonographic findings are suspicious for malignancy.

Keywords: cancer • FDG PET • fine-needle aspiration biopsy • PET • sonography • thyroid incidentalomas


Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Whole-body 18F-FDG PET is a noninvasive method and plays an important role in the evaluation for metastases in patients with various kinds of malignancies [1]. The use of PET is also increasing for cancer screening in healthy subjects with no previous history of malignant disease, particularly those at high risk of developing cancer [2, 3]. Thyroid incidentalomas with focal increased FDG uptake were found in 1.2–4.3% of patients or healthy subjects on PET examination in several studies [4–7]. Although some reports indicate that focal thyroid incidentalomas found on FDG PET have a high prevalence of thyroid malignancy [7–14], these results are still controversial [15, 16].

Confirmation of a high-uptake lesion in PET usually requires sonographically guided fine-needle aspiration biopsy (FNAB). During or before FNAB, sonography is also used to evaluate the thyroid nodule. Recently, the introduction of high-resolution sonography has made it possible not only to detect the thyroid nodules but also to substantially differentiate between benign and malignant lesions [17–22]. To our knowledge, however, no reports on the sonographic analysis of focal thyroid incidentalomas found on FDG PET have been published. Accordingly, the purpose of this study was to evaluate the risk of malignancy of thyroid incidentalomas found on FDG PET and the diagnostic accuracy of sonography for differentiating benign from malignant focal thyroid lesions incidentally found on FDG PET.


Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects
The institutional review board at our institution approved this study and determined that the approval and informed consent of the patients was not required for review of their images and records. From February 2002 to September 2006, 14,434 patients underwent combined sonography and sonographically guided FNAB at our institution. A retrospective observational study was conducted with data prospectively collected. Among the data, 90 consecutive focal thyroid lesions in 88 patients were aspirated because of focal radiotracer uptake observed on FDG PET. The final status of focal thyroid lesions was established by cytology or surgical pathology. Three patients were excluded because of insufficient samples on cytology and no further pathologic evaluation. Ultimately, this study included 87 focal thyroid lesions in 85 patients (67 women and 18 men). The interval between PET and FNAB was less than 90 days for most patients (range, 0–280 days; mean, 31.8 days). In four patients, however, the interval between PET and FNAB was 123, 135, 140, and 280 days. The 85 patients underwent FDG PET for the following reasons: cancer staging before treatment in 48, localization of recurrent disease in 28, primary site evaluation for unknown primary malignancy in two, and cancer screening in seven presumptively healthy subjects with no previous history of malignancy. Patient age ranged from 22 to 85 years (mean age, 55.8 years). The mean lesion size was 16.7 mm (range, 4–50 mm).

PET Method
All patients fasted for at least 4 hours and had a serum glucose level less than 140 mg/dL before the IV injection of FDG. Scanning was initiated 60 minutes after administration. Images from the neck to the proximal thighs were obtained either on a GE PET scanner (GE Advance, GE Healthcare) with a spatial resolution of 5 mm in the center of the field of view or on a Philips PET system (Allegro, Philips-ADAC Medical Systems) with a spatial resolution of 5.3 mm in the center of the field of view. For the GE Advance scanner, approximately 370 MBq of FDG was injected IV and PET was performed at 5 minutes per bed position in a 2D mode. The Allegro scanner acquired data in a 3D mode after the IV administration of 5.18 MBq of FDG. Transmission scans (3 minutes per bed position) using 68Ge for the GE Advance scanner or 137Cs for the Allegro scanner were obtained to correct for nonuniform attenuation correction. Transmission scans were interleaved between the multiple emission scans for the Allegro scanner. The obtained images were reconstructed using an iterative reconstruction algorithm, specifically either the ordered-subset expectation maximization (OSEM) for GE Advance or the low-action maximal likelihood algorithm (RAMLA) for Allegro.

Interpretation and Analysis of FDG PET Images
Either one of two experienced nuclear medicine physicians, unaware of other clinical or imaging information, interpreted the FDG PET images qualitatively by visual inspection on a high-resolution computer screen. Special attention was paid to FDG uptake in the thyroid glands. Focal thyroid uptake was defined as FDG uptake in less than one lobe. FDG uptake was considered abnormal on visual analysis when activity was substantially greater than that in the mediastinal blood on attenuation-corrected images. Regions of interests were drawn for quantification of FDG uptake on the visible lesions with increased radiotracer uptake, and the maximum standard uptake value (SUV) was semiquantitatively analyzed according to the following equation: SUV = A / (ID / BW), where A is the decay-corrected activity in tissue (in millicuries per milliliter), ID is the injected dose of FDG (in millicuries), and BW is the patient's body weight (in grams).

High-Resolution Thyroid Sonography
Sonograms were available from all patients. Sonography was performed using a 7- to 15-MHz linear array transducer (HDI 5000, Philips Medical Systems), an 8- to 15-MHz linear array transducer (Acuson Sequoia, Siemens Medical Solutions), or a 5- to 12-MHz linear array transducer (iU22, Philips Medical Systems) for evaluation of the thyroid gland and the neck. With the use of the HDI 5000 or iU22 machine, compound imaging was performed in all cases. Before FNAB, real-time sonography were performed by one of three radiologists with 4, 6, and 10 years of experience in thyroid imaging who knew the PET result at the time of sonography and sonographically guided FNAB.

Interpretations of sonography were prospectively entered into a computer database for clinical use. Each lesion was described using the sonographic features, including the internal component, echogenicity, margin, calcifications, and shape. We classified the nodules on the basis of previous criteria suggested by Kim et al. [18]. The internal component was defined as either solid, mixed, or cystic. A mass with mixed components meant the mass had a solid and a cystic component; sonography of masses with mixed components was evaluated on the basis of the internal solid component. Malignant sonographic features were defined as marked hypoechogenicity (lower echogenicity than the surrounding strap muscle), microlobulated or irregular margin, microcalcifications, and a taller-than-wide shape (i.e., greater in its anteroposterior dimension than its transverse dimension). Thyroid nodules were considered suspicious for malignancy if one of these findings was present on sonography. Our sonographic features were based on previous published criteria [18]. The sonography results, grouped into "suspicious for malignancy" and "probably benign," were compared with those of the final cytopathology reports to calculate the value of the test in diagnosing malignancy.

Sonographically Guided Fine-Needle Aspiration
After sonographic evaluation of the thyroid gland, sonographically guided FNABs were performed by the same radiologists, who evaluated the thyroid gland by sonography. In our institution, sonographically guided FNABs were performed of the thyroid nodule with focal uptake lesion seen on FDG PET. Sonographically guided FNAB was performed with a 23-gauge needle attached to a 20-mL disposable plastic syringe and aspirator by five radiologists specializing in thyroid imaging. Each lesion was aspirated at least twice. Materials obtained from the aspiration biopsy were expelled onto glass slides and smeared. All smears were placed immediately in 95% alcohol for Papanicolaou staining. The remainder of the material was rinsed in saline for processing as a cell block. Additional special staining was made on a case-by-case basis according to the cytopathologist's needs. The interpreting cyto pathologists were unaware of the sonographic diagnosis and the PET results.

Statistical Analysis
We evaluated the risk of malignancy in focal thyroid nodules with FDG PET uptake and its association with maximum SUV using logistic regression. A receiver operating characteristic (ROC) curve analysis was also performed to compare the accuracy of the maximum SUV to differentiate benign from malignant thyroid lesions. The kappa test and logistic regression were used to compare the two subgroups created by sonographic classifications for benign and malignant thyroid lesions. Statistical significance was assumed when the p value was less than 0.05. Statistical analysis was performed using the SPSS software package (SPSS).


Results
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 Materials and Methods
 Results
Discussion
 References
 
Of 87 focal thyroid lesions, 42 (48.3%) were malignant lesions and 45 were benign focal thyroid lesions based on cytopathologic results. Thirty-five (37 focal thyroid lesions) of 85 patients underwent surgery because of a malignant FNAB result (n = 32), insufficient samples at FNAB but suspicious sonography features (n = 2), and patient anxiety (n = 3). The remaining 50 patients did not undergo surgery. In those cases, we considered papillary carcinoma (n = 7) on cytology to be a malignant result, adenomatous goiter (n = 26), negative for malignancy (n = 15), and Hürthle cell change (n = 2) on cytology to be a benign result.


Figure 1
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  		Fig. 1 —Comparison of standard uptake values (SUVs) for benign and malignant focal thyroid lesions.

 
The average maximum SUV of the malignant nodules was 7.6 ± 8.09 (95% CI, 5.34–18.55), which was not significantly higher than that of the benign lesions (5.98 ± 5.11 [4.35–13.64]) based on logistic regression (Fig. 1). When the maximum SUV was used to differentiate benign from malignant focal thyroid lesions for the ROC curve analysis, the area under the curve (AUC) of PET was 0.553 (Fig. 2).


Figure 2
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  		Fig. 2 —Receiver operating characteristic curve of PET performance when maximum standard uptake value (SUV) is applied to differentiate benign and malignant focal thyroid lesions. Area under curve is 0.553.

 
The 87 thyroid nodules were divided into 49 suspicious malignant lesions and 38 probably benign nodules according to the sonographic features (Table 1). Of 49 lesions that showed suspicious sonographic findings, 37 (75.5%) revealed malignancy on cytopathology (Figs. 3A, 3B, and 3C). Thirty-eight showed probably benign sonographic findings, and only five (13.2%) lesions revealed malignant results (Figs. 4A, 4B, and 4C). A significant difference was seen between the two groups in the percentage of malignancy according to the kappa test ({kappa} = 0.675, p < 0.001) and logistic regression (odds ratio = 26.2, p = 0.001).


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  		TABLE 1: Cytopathologic Results and Sonographic Diagnoses of 87 Focal Thyroid Incidentalomas with Radiotracer Uptake on PET

 

Figure 3
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  		Fig. 3A —Papillary thyroid carcinoma in 58-year-old woman. Axial 18F-FDG PET scan shows focal radiotracer uptake in right thyroid gland.

 

Figure 4
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  		Fig. 3B —Papillary thyroid carcinoma in 58-year-old woman. Transverse (B) and longitudinal (C) sonograms show irregular tall hypoechoic mass in lower pole of right thyroid gland.

 

Figure 5
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  		Fig. 3C —Papillary thyroid carcinoma in 58-year-old woman. Transverse (B) and longitudinal (C) sonograms show irregular tall hypoechoic mass in lower pole of right thyroid gland.

 

Figure 6
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  		Fig. 4A —Adenomatous goiter in 55-year-old woman. Axial 18F-FDG PET scan shows focal radiotracer uptake in right thyroid gland.

 

Figure 7
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  		Fig. 4B —Adenomatous goiter in 55-year-old woman. Transverse (B) and longitudinal (C) sonograms show well-circumscribed ovoid isoechoic mass in mid pole of right thyroid gland.

 

Figure 8
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  		Fig. 4C —Adenomatous goiter in 55-year-old woman. Transverse (B) and longitudinal (C) sonograms show well-circumscribed ovoid isoechoic mass in mid pole of right thyroid gland.

 


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Thyroid nodules are common; they are found in 4–8% of adults by palpation and in 30–50% on sonography [23–25]. Data from autopsy studies have shown that the true prevalence of thyroid nodules is approximately 50% in autopsies of patients with no known thyroid disease [26]. Incidentally discovered thyroid lesions have become increasingly common with the development and more frequent use of highly sensitive imaging techniques, including sonography, CT, and MRI. Although thyroid nodules are commonly detected incidentally during CT or MRI of the head and neck, as well as of the chest, the differentiation of benign from malignant lesions is impossible using these techniques unless invasion into adjacent structures is seen [27]. On the other hand, high-resolution sonography is superior to physical examination and CT or MRI for detecting and characterizing thyroid nodules. Many studies have detailed the sonographic characteristics of thyroid nodules that suggest malignancy [17–22].

FDG PET is increasingly used in the diagnostic workup and follow-up of patients. We could not calculate the incidence of thyroid incidentalomas on FDG PET because we included only thyroid incidentalomas that underwent sonographically guided FNAB. However, thyroid incidentalomas with focal increased FDG uptake were found in 1.2–4.3% of patients or healthy subjects on PET examinations according to several studies [4–7]. Although several authors have reported that FDG accumulation may vary in the normal thyroid gland and that diffuse or focal moderate to intense FDG activity in the thyroid gland may be normal [15, 16], recent studies (Table 2) have shown that focal thyroid incidentalomas with uptake on FDG PET have a high prevalence of thyroid malignancy [5–14]. We also observed a high rate of malignancy, approximately 48.3%. When focal thyroid FDG uptake is detected in patients with an underlying malignancy, primary thyroid cancer, not just metastatic lesions, should be considered [7, 10]. In our study, all 42 malignant thyroid lesions in 40 patients with an underlying malignancy were confirmed as primary thyroid cancer, not metastatic lesions.


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  		TABLE 2: Published Reports of Rate of Malignancy of Focal Thyroid Incidentalomas Found on 18F-FDG PET

 

To differentiate malignant from benign focal thyroid lesions on FDG PET, many researchers have evaluated the usefulness of maximum SUV [6, 8, 9, 12, 28]. Some studies have shown that the maximum SUV of malignant thyroid lesions is significantly higher than that of benign lesions [6, 9, 28], but others have found that the maximum SUV does not predict the benign or malignant nature of the lesion [8, 12, 14]. In the current study, we saw no significant difference in maximum SUV between benign and malignant nodules, although the average maximum SUV of the malignant nodules was higher than that of benign lesions. When the maximum SUV was used to differentiate benign from malignant focal thyroid lesions for the ROC curve analysis, the area under the curve for PET was 0.553, indicating that the maximum SUV alone is not sufficient to differentiate malignant from benign focal thyroid lesions. Other techniques are needed for better characterization of focal thyroid lesions on PET.

In this study, we have evaluated the sonographic features at the time of the sonographically guided FNAB of thyroid incidentalomas identified by FDG PET. At our institution, we use the classification suggested by Kim et al. [18] for differentiating benign from malignant thyroid nodule. Recently, Tae et al. [29] reevaluated the merit of this sonographic classification in the differentiation of malignant from benign nodules. They concluded that this classification is useful in the differentiation of malignant nodules from benign nodules not only because it is simple and has high sensitivity but also because it has high negative predictive value [29]. We have shown that analyzing sonographic features can help manage thyroid incidentalomas on PET. When thyroid incidentalomas on PET were characterized as probably benign lesions on sonography, only 13.2% (5/38) were malignant, whereas 75.5% (37/49) were malignant when the nodules showed sonographic findings suspicious for malignancy. These differences were statistically significant. Therefore, our data suggest that sonographic characterization is still useful after the incidental detection of thyroid nodules on PET, as it is on thyroid nodules seen on other techniques, although the risk of malignancy in focal thyroid incidentalomas detected on FDG PET is high.

Our study has several limitations. First, this study included only focal thyroid lesions that were biopsied by aspiration. Patients with focal incidentalomas on FDG PET who did not undergo FNAB were not included in the study population. The inclusion of only patients who underwent subsequent FNAB may have introduced a bias. However, it has been routine practice at our institution to biopsy a thyroid incidentaloma detected on PET, which reduces the selection bias in our study population. Many other studies [5, 6, 8, 9, 14] dealing with focal incidentalomas on FDG PET also display selection bias. Because all focal thyroid incidentalomas found on FDG PET could not be confirmed cytopathologically, several studies included some (14.7–71.4%) of the focal thyroid incidentalomas on FDG PET that were confirmed cytopathologically (Table 2). From this point of view, we thought that a selection bias of focal incidentalomas found on FDG PET was inevitable and so should not decisively diminish the meaning of this study. Second, a relatively large proportion (57.5%, 50/87) of final diagnoses were based only on cytology results without postoperative histology. Although sonographically guided FNAB has been widely accepted for the diagnosis of thyroid nodules because of its simplicity, safety, and high sensitivity [30], false-negative results do occur with the procedure [31, 32], resulting in missed malignancy. As in our study, many reports [8, 9, 14, 33] studying thyroid uptake on PET have regarded benign cytologic results to mean a benign lesion although it has not been surgically proven. In clinical practice, this limitation is unavoidable.

In conclusion, the probability (48.3%) of malignancy of focal thyroid incidentalomas found on FDG PET is high. The maximum SUV of thyroid cancer is not significantly higher than that of benign lesions. The probability (13.2%) of malignancy is much lower when the sonographic findings appear benign, as opposed to a significantly higher probability (75.5%) of malignancy when the sonographic findings are suspicious for malignancy.


References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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