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The Journal of Clinical Endocrinology & Metabolism Vol. 92, No. 5 1630-1634
Copyright © 2007 by The Endocrine Society

18F-Fluorodeoxyglucose Positron Emission Tomography Does Not Predict Malignancy in Thyroid Nodules Cytologically Diagnosed as Follicular Neoplasm

Jung Min Kim1, Jin-Sook Ryu1, Tae Yong Kim, Won Bae Kim, Gui Young Kwon, Gyungyub Gong, Dae Hyuk Moon, Seong Chul Kim, Suck Joon Hong and Young Kee Shong

Departments of Internal Medicine (J.M.K., T.Y.K., W.B.K., Y.K.S.), Nuclear Medicine (J.-S.R., D.H.M.), Pathology (G.Y.K., G.G.), and Surgery (S.C.K., S.J.H.), Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, Korea

Address all correspondence and requests for reprints to: Young Kee Shong, M.D., Ph.D., Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Pungnap-dong, Songpa-gu, Seoul 138-736, Korea. E-mail: ykshong{at}amc.seoul.kr.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Objective: The objective of this study was to evaluate the usefulness of 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) in predicting malignancy in thyroid nodules cytologically diagnosed as follicular neoplasm.

Patients and Methods: A total of 46 patients with thyroid nodules larger than 1 cm in diameter cytologically diagnosed as follicular neoplasm at Asan Medical Center (Seoul, Korea) were included. FDG-PET images were taken in all patients before surgical resection, and the maximum standardized uptake value (SUVmax) of each nodule was measured.

Results: FDG-PET showed hypermetabolic activity of all nodules compared with normal thyroid tissue. Thirty-six patients underwent surgery, whereas 10 refused immediate operation. Fifteen patients had cancer: 11 with follicular and two each with Hürthle cell and follicular variants of papillary cancer. Twenty-one patients had benign nodules: 11 follicular adenomas, eight adenomatous hyperplasias, and two Hürthle cell adenomas. SUVmax did not differ significantly between malignant and benign nodules (3.6 ± 3.5 vs. 3.4 ± 3.2; P = 0.83) or among subtypes of benign nodules (P = 0.23). However, SUVmax differed significantly among subtypes of malignant nodules (P = 0.02).

Conclusions: On FDG-PET, the glucose metabolic activities of benign thyroid follicular nodules were as high as those of malignant nodules. These findings suggest that FDG-PET has limited value for selecting candidates for surgery among patients cytologically diagnosed as follicular neoplasm.


   Introduction
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 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
CYTOLOGICAL DIAGNOSIS OF follicular neoplasms is performed when abundant follicular epithelial cells are present in sheets, microfollicles, or trabecular patterns with scanty or no colloid. These patterns, however, may be present in follicular adenomas, follicular carcinomas, nodular goiters, and follicular variants of papillary carcinoma (1). Thus, an additional test, which could differentiate malignant from benign nodules in the case of follicular neoplasm, would be of great use.

18F-fluorodeoxyglucose positron emission tomography (FDG-PET) has been used to differentiate malignant from benign tumors (2, 3, 4) and may be useful in the evaluation of thyroid nodules (5, 6). It is unclear, however, whether FDG-PET is suitable in the preoperative assessment of thyroid nodules after preoperative cytological diagnosis of follicular neoplasm. We therefore evaluated the usefulness of FDG-PET in the prediction of malignancy in thyroid nodules cytologically diagnosed as follicular neoplasm.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

All 46 consecutive patients with thyroid nodules greater than 1 cm in diameter cytologically diagnosed as follicular neoplasm at the Asan Medical Center (Seoul, Korea) from January 2005 to June 2006 were included. The 46 patients (seven men, 39 women) had a median age of 44 yr (range, 23–73 yr). Serum TSH was measured to rule out autonomous functioning nodules, and all patients were euthyroid. FDG-PET images were obtained from all before surgical resection. Surgery was recommended to all of the patients after thorough explanation about the condition. Those patients who refused immediate surgery were recommended to undergo close regular follow-up, including repeated fine-needle aspiration (FNA) and thyroid ultrasonography (USG). Written informed consent was obtained from each patient. This study was approved by the Institutional Review Board of the Asan Medical Center.

Diagnostic work-up of thyroid nodules

Thyroid USG was performed in all patients to confirm the presence and location of palpable nodule(s) and to locate other impalpable thyroid nodule(s) that required FNA based on their size (>1 cm) and appearance.

Forty-two patients had palpable thyroid nodule(s); thyroid USG showed that 29 patients had solitary nodules, whereas 13 patients had two or more nodules, all of which were solid. In 13 patients with two or more nodules, the largest palpable nodule was selected for this study.

Four patients had impalpable nodule(s), including those with nodule(s) identified by USG and referred to our hospital; three patients had solitary nodules, whereas one patient had three nodules. In this patient with multiple nodules, the largest solid nodule larger than 1 cm was evaluated by FNA. USG guidance was used in these four patients to confirm needle placement in each nodule.

FNA was performed by an experienced cytopathologist, and all aspirates were stained with Papanicolaou staining and reviewed by two expert cytopathologists (G.Y.K. and G.G.). Follicular neoplasm was cytologically diagnosed when high cellularity, scanty colloid, and microfollicular pattern were noted concurrently by two independent cytopathologists. Cases of diagnostic discordance were excluded. The results of the postoperative histopathological examination were compared with the preoperative cytology. Incidentally found papillary microcarcinomas were not considered in this analysis. In all cases, cytology slides were retrospectively reviewed after histological confirmation. Maximum diameter of nodules was measured at pathological examination.

The location of each nodule was compared with FDG-PET scan results to confirm the area of interest before final analysis.

FDG-PET

All patients were asked to fast for a minimum of 6 h, and serum glucose level was confirmed as less than 120 mg/dl before iv administration of 370 to 555 MBq of FDG through a peripheral vein. Sixty minutes later, regional neck PET images were acquired using a full-ring dedicated PET scanner (ECAT Exact HR+; Siemens-CTI, Knoxville, TN) with an axial field of view of 15.5 cm and a full-width at half-maximum at the center of the field of view of 4.2 mm. PET scans were obtained at 10 min per bed position for emission scanning and 5 min per bed position for transmission scanning. The PET images were reconstructed on a 128 x 128 matrix with a zoom factor 1.5 using an ordered-subsets expectation maximization algorithm for 16 subsets and two iterations with a 5-mm Gaussian filter. PET images were visually interpreted by two experienced nuclear physicians (J.-S.R. and D.H.M.) blind to the exact location and size of each nodule. For a semiquantitative analysis of metabolic activity, the volume of interest was placed around the thyroid nodular lesion, and the maximum standardized uptake value (SUVmax) based on lean body mass was calculated.

Statistics

All statistical tests were carried out using SPSS (version 12.0; SPSS Inc., Chicago, IL). The Mann-Whitney U test was used to compare maximum diameter and SUVmax of malignant thyroid nodules with those of benign thyroid nodules. The Kruskal-Wallis exact test was used to compare SUVmax among subtypes of malignant and benign nodules. The Spearman’s rank test was performed to determine the correlation of SUVmax with the maximum diameter of malignant or benign nodules. All tests were considered significant at P < 0.05.


   Results
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 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Of the 46 patients, 36 patients (five men, 31 women; median age, 44 yr; range, 25–73 yr) underwent lobectomy and isthmectomy. In addition to the main nodule, two patients each with malignant and benign nodules had occult papillary microcarcinomas. Among the 36 patients who underwent surgery, 15 were found to have malignant thyroid nodules after surgery (Table 1Go, subjects 1–15). Of these, 11 had follicular carcinomas and two each had Hürthle cell carcinomas and follicular variants of papillary carcinoma. After histological confirmation, completion thyroidectomy was performed in all patients with malignant disease. Twenty-one patients had benign thyroid nodules (Table 1Go, subjects 16–36), including 11 follicular adenomas, eight adenomatous hyperplasias, and two Hürthle cell adenomas. The mean age of patients with malignant and benign nodules was 46 ± 16 and 43 ± 11 yr, respectively. The maximum diameters in malignant and benign nodules (3.2 ± 2.1 cm vs. 3.1 ± 1.6 cm; Mann-Whitney U = 55.0; P = 0.89) did not differ significantly. Outliers seemed to be due to SUVmax (Table 1Go), because SUVmax was higher in larger nodules regardless of malignancy (see Fig. 4Go).


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  		TABLE 1. Results of FDG-PET and histopathology in patients with thyroid nodules cytologically diagnosed as follicular neoplasm

 

Figure 4
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  		FIG. 4. Correlation of SUVmax with the maximum diameter of nodules. Both malignant (filled squares) and benign nodules (open circles) showed correlations (Spearman r = 0.61; P < 0.001).

 
Ten patients refused surgery and chose regular follow-up. Of these, six patients underwent repeated FNA and thyroid USG with all patients still having indeterminate cytology. Although nodule size did not change during the short follow-up period, three patients showed progressive cystic change, and these nodules were considered benign. These six patients have undergone close regular followup. The remaining four patients were lost to follow-up.

Compared with normal thyroid tissue, all nodules showed hypermetabolic activity on FDG-PET. The time interval between FNA and FDG-PET was greater than 4 wk. The mean SUVmax in malignant nodules was 3.6 ± 3.5 (range, 0.9–15.0; representative cases, Fig. 1Go, A and B), whereas the mean SUVmax in benign nodules was 3.4 ± 3.2 (range, 1.2–16.2; representative cases, Fig. 1Go, C and D), and these differences were not significant (Mann-Whitney U = 153.0; P = 0.83; Fig. 2Go). We also compared SUVmax among subtypes of malignant and benign nodules (Fig. 3Go). Although there was no significant difference in SUVmax among subtypes of benign nodules (Kruskal-Wallis = 3.09; P = 0.23), the SUVmax among subtypes of malignant nodules differed significantly (Kruskal-Wallis = 5.98; P = 0.02). There was a significant correlation SUVmax with the maximum diameter of nodules when all nodules were analyzed irrespective of pathological findings (Spearman r = 0.61; P < 0.001; Fig. 4Go). We also observed a significant correlation SUVmax with maximum diameters, both of malignant (Spearman r = 0.74; P = 0.002) and benign (Spearman r = 0.52, P = 0.01) nodules.


Figure 1
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  		FIG. 1. FDG-PET images of malignant (A and B) and benign (C and D) thyroid nodules. Representative images were selected with similar FDG uptake by malignant and benign nodules. A, FDG-PET images of a 47-yr-old woman (subject 3 in Table 1Go) showing a lesion with increased FDG uptake (SUVmax = 1.3) in the right thyroid gland. Follicular thyroid carcinoma was confirmed by postoperative pathological examination. B, FDG-PET images of a 51-yr-old woman (subject 14 in Table 1Go) showing a lesion with increased FDG uptake (SUVmax = 6.1) in the right thyroid gland. Follicular variant of papillary carcinoma was confirmed by postoperative pathological examination. C, FDG-PET images of a 30-yr-old woman (subject 16 in Table 1Go) with mildly increased uptake in the right thyroid (SUVmax = 1.2). Postoperative pathological diagnosis was adenomatous hyperplasia. D, FDG-PET images of a 48-yr-old man (subject 35 in Table 1Go) with increased uptake in the left thyroid (SUVmax = 5.9). Hürthle cell adenoma was confirmed by postoperative pathological examination.

 

Figure 2
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  		FIG. 2. SUVmax of malignant and benign nodules. The difference between malignant and benign nodules was not significant (P = 0.83). The line shows the median value of SUVmax.

 

Figure 3
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  		FIG. 3. SUVmax among subtypes of malignant and benign nodules. The line shows the median value of SUVmax. SUVmax among subtypes of malignant nodule (P = 0.02), but not benign nodules (P = 0.23), differed significantly.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The diagnosis of follicular neoplasm is made in approximately 20% of thyroid nodules by FNA (7). The malignant potential of follicular neoplasms, however, can rarely be determined by cytological evaluation alone; thus, these lesions are generally classified as cytologically indeterminate, and most patients are advised to undergo surgical resection (7). Because cells from follicular adenomas and follicular carcinomas may appear identical, only the identification of capsular or vascular invasion on histological specimens can diagnose cancer.

Although malignancy is found in approximately 20% of follicular nodules classified as indeterminate on FNA (8), we detected thyroid cancer in 15 of 36 (42%) patients. Other studies, including one in Korean populations, have reported thyroid cancer in 42 to 47% of patients with cytological diagnosis of follicular neoplasm (9, 10). The higher incidence reported in these studies may have been due to the stricter criteria for the diagnosis of follicular neoplasm when follicular cells are seen on aspirates in our institute or to ethnic differences. Due to the high rate of malignancy in patients with cytological diagnosis of follicular neoplasm in our institute (10), surgery has been strongly recommended to every patient.

In this study, we evaluated whether FDG-PET is useful for predicting malignancy in thyroid nodules cytologically diagnosed as follicular neoplasm. We found that the glucose metabolic activities of benign nodules were as high as those of malignant nodules. Moreover, we did not find any SUVmax cutoff value for differentiating between malignant and benign nodules. These findings suggest that FDG-PET is not helpful in differentiating between malignant and benign nodules and therefore has only limited value in preoperative evaluation of indeterminate thyroid nodules.

Previously, studies examining the usefulness of FDG-PET in differentiating malignant from benign nodules and in the preoperative evaluation of thyroid nodules have yielded conflicting results. Only one study showed no overlap between malignant and benign nodules (11), whereas most found considerable overlap in their glucose metabolic activities (5, 6, 12, 13, 14, 15, 16). Several studies found a significant difference in mean on FDG-PET between malignant and benign nodules (5, 6, 12, 13, 14, 15) with most benign nodules having low glucose uptake (15), suggesting that mean SUV can be used to differentiate malignant from benign nodules. The SUV cutoff value was found to differ, being 2.0 (6), 2.5 (12), and 5.0 (14). Other studies have suggested that FDG-PET has a limited role in differentiating malignant from benign nodules because benign nodules could also accumulate FDG (16). These studies, however, had several limitations, mostly stemming from small patient numbers (11, 13) and the inclusion of benign nodules such as Hürthle cell adenomas (6) and chronic thyroiditis (13) in the section of SUV of malignant nodules decided by using cutoff values.

Our findings were inconsistent with those of studies that included subgroup analyses in evaluating the usefulness of preoperative FDG-PET in cytologically indeterminate thyroid nodules (6, 14, 15). These studies reported that, although there was a considerable overlap in glucose metabolic activities of malignant and benign nodules, FDG-PET was useful for differentiating malignant from benign nodules due to its high negative predictive value for malignant nodules (6, 14, 15). In contrast, we found that FDG was accumulated by all benign nodules.

These findings on the usefulness of FDG-PET for prediction of malignancy in thyroid nodules are confusing. However, they may be due to the low SUVmax of malignant thyroid nodules. Thus, follicular carcinomas may be associated with the low SUVmax of malignant thyroid nodules. The mean SUVmax of follicular carcinomas was lower than that of Hürthle cell carcinomas and follicular variants of papillary carcinoma as shown in Fig. 3Go, and there was a significant difference in SUVmax among subtypes of malignant nodules. The numbers of patients, however, were too small for statistical significance to be attained. SUVmax of small malignant lesions, including small papillary carcinomas, may also be low due to partial volume effects (6, 17). Actually, we measured SUVmax to avoid partial volume effect. This effect, however, is negligible in tumors larger than 1.5 cm in diameter. Although the maximum diameter of all malignant nodules in this study was larger than 1.5 cm, we observed a significant correlation of the SUVmax with the maximum diameter of nodules (17). The cause of this phenomenon is unclear. In addition, benign thyroid nodules could have relatively increased FDG uptake. Hürthle cell adenomas have been reported to have higher SUVmax than other benign conditions (6, 14, 15, 18), although we did not observe this in the present study. Although lesions involving chronic thyroiditis and Graves’ disease have high SUVmax (19), these lesions usually demonstrate diffuse FDG uptake. None of the patients in our study showed diffuse FDG uptake, and none had chronic thyroiditis or Graves’ disease in pathological reports. Although the inflammatory or reactive changes after FNA can influence subsequent PET scans, the interval between FNA and PET in our study was at least 4 wk, making this possibility unlikely. The expression of glucose transporter proteins (GLUTs) has been reported to vary between malignant and benign thyroid nodules (20), suggesting that these nodules can take up a variable amount of FDG. Our preliminary results show no correlation between GLUT 1 expression with SUVmax of nodules, perhaps because differentiated carcinomas have lower GLUT 1 expression than undifferentiated carcinomas (21, 22). Thus, SUVmax could not be used to differentiate between benign adenomas and differentiated carcinomas.

In this study, 14 patients had multiple thyroid nodules. In 10 patients with multiple nodules, nodule(s) other than the aspirated nodule were located in the contralateral lobe, and there was no difficulty in correlation of the hot lesion on PET scan with the location of the aspirated nodule. In the remaining four patients with multiple nodules, nodules were located in the ipsilateral lobe. Thus, we subdivided the thyroid area of the PET scan into the upper and lower portions to correlate the location of the nodule(s). Although we easily correlated the hot lesion on PET scan with the location of the aspirated nodule, there might be an error in a small portion of patients with multiple nodules.

In conclusion, we found that the glucose metabolic activities of benign thyroid follicular nodules were as high as those of malignant nodules on FDG-PET. FDG-PET seems to have limited value for selecting candidates for surgery among patients with cytological diagnosis of follicular neoplasm.


   Footnotes
 
The abstract was presented at the 77th Annual Meeting of the American Thyroid Association, Phoenix, Arizona, October 11–15, 2006.

Disclosure Statement: The authors have nothing to disclose.

First Published Online February 6, 2007

1 J.M.K. and J.-S.R. should be considered joint first authors. Back

Abbreviations: FDG-PET, 18F-fluorodeoxyglucose positron emission tomography; FNA, fine-needle aspiration; GLUT, glucose transporter protein; SUV, standardized uptake value; SUVmax, maximum SUV; USG, ultrasonography.

Received October 23, 2006.

Accepted January 30, 2007.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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