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10.1245/s10434-006-9181-y
Annals of Surgical Oncology 14:239-247 (2007)
© 2007 Society of Surgical Oncology
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Original Article

FDG-PET Detected Thyroid Incidentalomas: Need for Further Investigation?

Chandrakanth Are, MD1, John F. Hsu, DO2, Heiko Schoder, MD3, Jatin P. Shah, MD4, Steve M. Larson, MD3 and Ashok R. Shaha, MD4

1 Department of Surgical Oncology, Memorial Sloan-Kettering Cancer Center, 1233 York Avenue, 16 I, New York, New York, 10021, USA
2 Department of Surgery, Wyckoff Heights Medical Center, 374 Stockholm Street, Brooklyn, New York, 11237, USA
3 Department of Radiology, Nuclear Medicine Service, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York, 10021, USA
4 Department of Head and Neck Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York, 10021, USA

Correspondence: Address correspondence and reprint requests to: Ashok R. Shaha, MD; E-mail: shahaa{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Incidental thyroid abnormalities are increasingly detected in patients undergoing PET scans. The aim of this study was to review our experience with the management of PET detected thyroid incidentalomas in a large single institution series.

Methods: All PET scans performed from May 2003 to July 2005 were reviewed and patients with incidental thyroid abnormalities were identified. From this group, patients that underwent further investigation were analyzed. Data relating to PET scan findings, FNA diagnoses, operative details, and histopathology was reviewed.

Results: In 8,800 patients, 16,300 PET scans were performed of whom 263 patients (2.9% of patients and 1.6% of PET scans) had findings positive for thyroid abnormality. Thyroid malignancy was noted in 42% (24 patients) of the 57 patients that underwent FNA. In the group of 27 patients that were subjected to operative intervention, 74% (20 patients) were noted to have a malignant diagnosis. The final histopathology revealed primary thyroid carcinoma in all these 20 patients (19 patients with papillary carcinoma and one patient with primary thyroid lymphoma). The factors that correlated with an increased risk of malignancy were the presence of physical finding (p = 0.01) and focal (p < 0.01) or unilateral uptake (p < 0.01) on PET scan. The average SUV was not useful in differentiating benign (9.2) from malignant lesions (8.2, p = 0.7).

Conclusions: PET detected incidental thyroid abnormalities are rare. In patients with positive PET scan findings and suspicious features, the incidence of primary thyroid malignancy is very high. These patients warrant further investigation followed by possible operative intervention.

Abbreviations: FDG-PET scan • Thyroid • Incidentalomas • Risk of malignancy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Positron emission tomogram scans with 18 F-flourodexoyglucose (FDG-PET) are increasingly performed in the management of patients with malignant conditions of various organ systems. There are several reports documenting incidentally detected thyroid lesions on PET scans (PETI) in patients with no known prior history of thyroid disease.1–6 PET scan has also been shown to be very reliable in the diagnosis and follow up of patients with recurrent or metastatic thyroid carcinoma of all subtypes.7–12 The sensitivity of PET scan in detecting thyroid malignancy increases the significance of these incidentally detected thyroid lesions.

The actual prevalence of malignancy in patients with PETI and their optimal management is still controversial. Some reports have noted a high incidence of malignancy in patients with PETI which stresses the importance of subjecting these patients to further extensive investigations.1,3,6 In contrast, other authors have noted that the majority of the patients with PETI harbor a benign diagnosis and have suggested that not all patients with PETI need further evaluation.2 From these reports, it is therefore unclear as to which patients with PETI should undergo further investigation. To subject all patients with PETI to further evaluation can lead to unnecessary expense and investigations. The paucity of reports and small number of patients in these series make it difficult to determine the true prevalence of malignancy and to reach any conclusion on a reliable diagnostic algorithm for the management of PETI.

The aim of our study was to determine the prevalence of malignancy in patients with PETI in a large series of patients from a single institution. In addition, we hope to elucidate reliable criteria suggestive of malignancy that may help in determining which patients with PETI should undergo further investigations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All PET scans performed in our Department of Nuclear Medicine from May 2003 to July 2005 were reviewed and the study was approved by the Institutional Review Board. PET scans were usually performed as part of extent of disease work up for various primary malignancies. From these, only PET scans with any incidentally detected thyroid abnormality were identified. Thyroid abnormalities were defined as the presence of any abnormal uptake and divided into focal (Figs. 1Go and 2Go) or diffuse (Fig. 3Go) and unilateral (Figs. 1Go and 2Go) or bilateral uptake (Figs. 3Go and 4Go). Focal and diffuse uptake was defined as the presence of a focal or diffuse abnormality involving any portion of the thyroid gland. Unilateral or bilateral uptake was defined as the presence of any abnormality involving one or both lobes (focal or diffuse) of the thyroid gland. The average SUV values were also obtained for each patient with PET scan abnormality.


Figure 1
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  		FIG. 1. 42 y.o. female patient with primary lymphoma. The FDG-PET revealed focal and unilateral uptake with SUV of 5.4. The patient underwent total thyroidectomy with a final diagnosis of Hurthle cell adenoma.

 

Figure 2
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  		FIG. 2. 71 y.o. female patient with primary anal cancer. The FDG-PET revealed focal and unilateral uptake with SUV of 4.2. The patient underwent total thyroidectomy with a final diagnosis of follicular variant of papillary thyroid cancer.

 

Figure 3
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  		FIG. 3. 57 y.o. male patient with primary small cell cancer of lung. The FDG-PET revealed diffuse uptake with SUV of 11.7. The patient underwent FNA with a final diagnosis of metastatic involvement of the thyroid.

 

Figure 4
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  		FIG. 4. 67 y.o. male patient with primary tongue cancer. The FDG-PET revealed bilateral uptake with SUV of 8.5. The patient underwent FNA with a final diagnosis of chronic lymphocytic thyroiditis.

 
The age, demographics, physical findings (presence of palpable mass), and location of primary lesion for all patients with abnormal PET scan findings were collected. In patients that underwent fine needle aspiration cytology (FNA), the diagnoses were categorized as benign, malignant, and indeterminate. The extent of operation (lobectomy vs total thyroidectomy) and the final histopathological diagnosis were documented in patients that underwent operative intervention. The significance of age, gender, physical finding, and type of uptake on PET scan were correlated to the risk of malignancy in patients with a tissue diagnosis.

PET Imaging
All patients fasted for at least 6 hours prior to tracer injection. Upon arrival in the nuclear medicine clinic, 15 mCi (555MBq) of18 FDG was injected intravenously. PET imaging started following a 60 minute uptake period, during which time the patients rested quietly in a reclined chair. Plasma glucose was measured and found to be in the acceptable range (< 200 mg/dl) in all patients. All studies were performed on integrated PET/CT scanners: Biograph (Siemens, Hoffman Estates, IL) or Discovery LS (GE Medical Technologies, Waukesha, WI). These machines combine state of the art CT and PET.13,14 Following scout view (120–140 kVp, 30 mAs), dedicated low dose CT and PET (5 min / bed position) of the head and neck were acquired from the mid skull to the thoracic inlet in an "arms-down" position. CT parameters were as follows: Biograph – 130 kVp, effective mAs 50, 5 mm scan width, and 12 mm feed / rotation; Discovery – 140 kVp, 80 mAs, 5 mm scan width, 4.25mm interval in high-sensitivity mode with 15 mm/rotation table speed. Subsequently, low dose CT and PET of the torso were acquired in "arms up" position and image acquisition from the thoracic inlet to the floor of the pelvis (Biograph in 3D mode with 3–4 cm overlap and Discovery LS in 2D mode with 1–2 cm overlap between the FOVs). PET images were reconstructed using iterative algorithms. The CT data were used for attenuation correction of PET emission images.

Image Interpretation
All data were reviewed on a computer display. PET images were first reviewed in 3 orthogonal planes (transaxial, coronal, sagittal) and a multi-intensity projection (MIP) image. Afterwards, CT, PET, and a PET/CT fusion image were displayed simultaneously. Non-attenuation corrected PET images were also reviewed. Image interpretation was based on visual and semiquantitative analysis using the attenuation corrected PET emission images. FDG uptake in the thyroid gland, which was greater than background activity in adjacent tissues and blood pool, was classified as unifocal, multifocal, or diffuse. For semiquantitative analysis, circular regions of interest (ROI) were placed over these thyroid foci and the maximum standardized uptake value (SUV), normalized to body weight, was measured.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A total of 16,300 PET scans were performed with some patients undergoing repeat imaging. The number of patients that underwent PET scans during the study period was 8,800. Of these, 263 patients with no known prior history of any thyroid disorder were noted to have incidental abnormalities in the thyroid gland. (1.6% of total PET scans performed and 2.9% of total patients examined). 57 patients (21%) with positive PET scan findings were investigated further with the help of FNA. A total of 27 patients, 10.2% (25 patients with FNA and 2 patients without FNA), were subjected to operative intervention.

Findings in Patients with PETI
The median age of all 263 patients with PETI was 63 (± 13) years and the male: female ratio was 31 vs 69%. In 25 patients (9%), there was clinical evidence of physical findings involving the thyroid gland. 101 patients (38%) and 162 patients (62%) were noted to have focal and diffuse uptake respectively on the PET scan. In 124 patients (47%), the abnormalities were unilateral in nature. The abnormal findings involved the right lobe in 59 patients (22%), left lobe in 65 patients (24%) and both lobe of the thyroid in the remaining 139 patients (52%).

Findings in Patients with PETI and FNA
57 patients (21%) with positive PET scan findings were subjected to FNA to determine the diagnosis. The median age of this group was 61.1 years (± 12) with a male: female ratio of 31 vs 69%. The incidence of physical findings was seen in a greater percentage of patients (10 patients - 17%). The incidence of focal uptake (42 patients - 73%) and unilateral uptake (47 patients - 82%) was higher than the entire cohort of patients with PETI. PET scan findings were localized to the right lobe, left lobe and both lobes in 21 patients (36%), 26 patients (45%) and 10 patients (18%), respectively. The FNA diagnoses in this group of patients were as follows: benign - 29 pts (50%), malignant 24 patients (42%), and indeterminate - 4 patients (7%).

Findings in Patients with PETI that underwent Operative Intervention
A total of 27 patients (10.2%) with positive PET scan findings underwent operative intervention. The mean age and male: female ratio was 58 years and 22:78%, respectively. A total thyroidectomy was performed in 20 patients with the remaining undergoing lobectomy only. A greater number of patients were noted to have abnormal findings on physical examination [7 patients (25%)]. The majority of patients that underwent operative intervention were noted to have PET scan findings suggestive of focal (23 patients - 85%) and unilateral uptake (24 patients - 88%). The PET scan abnormalities involved the right and left lobes in 10 patients (37%) and 14 patients (51%), respectively.

Overall Prevalence of Malignancy
The prevalence of malignancy was 42% (24 out of 57 patients) and 74% (20 out of 27 patients) in patients that underwent FNA or operative intervention respectively. The distribution of malignant diagnoses in the 20 patients with available histopathology was as follows: papillary carcinoma (12 patients), follicular variant of papillary thyroid carcinoma (7 patients), and primary lymphoma involving the thyroid (1 patient). Seven patients with a benign diagnosis [Hurthle cell adenoma (5 patients) and nodular hyperplasia (2 patients)] were operated upon for a presumed malignancy based on the findings on FNA.

Prevalence of Malignancy in Patients with PETI based on Risk Factors: (Table 1Go)
The prevalence of malignancy was correlated to the known risk factors associated with thyroid carcinoma and the type of PET scan abnormality. There was a higher prevalence of malignant diagnoses in patients > 50 years of age and male sex although these findings were not significant. (p = 0.39 and 0.14). The risk of malignancy was higher in the presence of physical findings. (24% vs 6.3%, p = 0.01). Focal uptake was associated with a higher prevalence of malignancy when compared to patients with diffuse uptake (18% vs 1.2%, p < 0.01). Similarly, patients with unilateral uptake were more likely to harbor a malignant diagnosis. (15% vs 2.1%, p < 0.01). There was no difference in the average SUV for patients with benign and malignant diagnoses that underwent operative intervention. The average SUV for benign and malignant diagnoses was 9.2 (± 6.9 with a range of 4.1 to 21.3) and 8.2 (± 7 with a range of 2.9 to 27), respectively (p = 0.7).


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  		TABLE 1. Prevalence of malignancy in patients with PETI based on risk factors
 
An assessment of our practice in the management of PETI revealed some trends (Table 2Go). In patients with PETI and abnormal physical finding, we are more likely to pursue further investigation. In addition, patients with focal or unilateral uptake are investigated more aggressively with FNA or operative intervention. In contrast, more patients with diffuse or bilateral uptake were managed conservatively.


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  		TABLE 2. Trends in investigations based on risk factors
 
The majority of patients with PETI had primaries involving the gastrointestinal tract, respiratory tract, breast, and hematological system (Table 3Go). The same groups of patients with suspicious features were investigated further to an equal extent with FNA or operative intervention. The prevalence of malignancy was noted to be higher in patients with primaries involving the head and neck (excluding thyroid), breast, and gastrointestinal tract.


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  		TABLE 3. Location of primary lesion
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The normal and healthy thyroid gland shows very low FDG uptake and is usually not visualized on PET imaging. Abnormal uptake of FDG in the thyroid gland could be due to benign15–18 or malignant conditions.1,3,5 Although benign conditions such as Graves’ disease16 and nodular goiters13 can be associated with increased FDG uptake, abnormal PET scan findings are usually thought to be due to a malignant process.1,3,5 PET scan has shown to be very reliable in the surveillance of patients with recurrent or metastatic thyroid cancer.7,9,10,12,19,20 In fact, PET scan has been shown to be very sensitive in detecting recurrent disease even when I-131 scans are negative.8 This high sensitivity of PET in detecting recurrent or metastatic thyroid malignancies underscores the clinical significance of PET detected thyroid incidentalomas.

Incidentally detected thyroid abnormalities are increasingly detected with the routine use of radiological investigations.21 Certain findings such as micro-calcifications, irregular margins, and incomplete halo on ultrasound examination increase the likelihood of malignancy.22,23 Although there are no specific findings to suggest malignancy on CT and MRI, invasion of surrounding structures is an ominous abnormality. Due to its relatively recent introduction, there are still no definitive PET criteria to help diagnose malignancy in thyroid incidentalomas. This assumes importance when one realizes that PET scans are increasingly performed in the management of patients with malignancies. Some authors have suggested the level of SUV1,2,5 may help in differentiating benign from malignant thyroid incidentalomas seen on PET scan. In fifteen patients that had a tissue diagnosis, Cohen et al. noted that the average SUV to be higher in malignant lesions (6.92 ± 1.54) than for benign lesions (3.37 ± 0.21), whereas others have reported no difference in SUV between benign and malignant nodules.3,24 The quality of uptake on PET scan (focal versus diffuse) has been documented by some to help isolating benign from malignant lesions3,5 although this has not been confirmed in a recent report.2 Similarly, the importance of the presence of physical finding in this group of patients is not clarified. The paucity of studies and the small number of patients in the published reports on this relatively new and rare entity make it difficult to reach any conclusions. The aim of our study was to determine the prevalence of malignancy in a large series of patients and elucidate criteria that may help in selecting appropriate patients for further investigations.

The prevalence of PETI was 2.9% (of 8,800 patients) and 1.6% (of 16,300 scans), which is similar to what has been previously reported in the literature1,3 (Table 4Go). These small numbers help to negate the fear of an alarming increase in the incidence of PETI.4 At the same time, although the prevalence of PETI is low, the increasing utilization of PET scan will lead to larger number of patients being referred to our clinics. In addition, these findings are similar to the incidence of PETI in normal healthy subjects.2,5 Although the prevalence of PETI may be low, in patients with a tissue diagnosis, the prevalence of malignancy was high ( 42% with FNA and 74% with operative intervention). The results of our study are in concurrence with the findings of other publications on the issue (Table 4Go).


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  		TABLE 4. Summary of studies on Positron Emission Tomogram Detected Thyroid Incidentalomas (PETI)
 
The findings that were noted to be useful in isolating patients with malignancy were the presence of physical finding and the detection of focal or unilateral uptake on PET scan. Although the presence of physical finding was noted only in 7% of patients with PETI, this number increased to 25% of the patients that were operated upon. In the entire cohort of 263 patients with PETI, the incidence of malignancy was much higher in the presence of physical finding (24% versus 6.3% in the absence of physical finding, p = 0.01). The detection of focal uptake on PET scan significantly increased the risk of malignancy (18%) when compared to patients with diffuse uptake (1.2%, p < 0.01). Of the 162 patients with diffuse uptake, only two patients (1.2%) were noted to harbor malignancy on tissue diagnosis. These findings are similar to the results documented by Kang et al.5 In their series of 1330 patients, eight patients were documented to have diffuse uptake of whom seven were noted to have chronic thyroiditis.5 Similarly, the risk of malignancy increased from 1.4 % with bilateral uptake when compared to 15% with unilateral uptake (p < 0.01). These findings suggest that the risk of malignancy is extremely low in patients with diffuse or bilateral uptake on PET scan. The high risk of malignancy with focal or unilateral uptake should prompt further investigation even in the absence of physical findings as long as it is within the context of the extent of disease of the primary malignancy.

In contrast, the well known clinical risk factors for thyroid cancer such as age >50years and male sex did not have a bearing on the prevalence of malignancy. Although patients > 50 years of age had a higher prevalence of malignancy, this was not statistically significant. The lack of impact of age on the risk of malignancy could be due to small number of patients in the study. Similarly, the SUV did not correlate with the risk of malignancy. In the 27 patients that underwent operative intervention, the average SUV was noted to be 8.2 and 9.2 (p = 0.7) for malignant and benign conditions respectively. This could be due to various reasons. Hurthle cell adenomas are known to be associated with high SUV.25 In our study, five out of seven patients with a benign diagnosis had Hurthle cell adenoma and the average SUV was greater than 5 in all but one. In addition, small papillary thyroid carcinomas are known to have low SUV or the SUV may be underestimated due to partial volume effects. Six out of twelve patients with papillary thyroid cancer in the present study had SUV less than 5.25 These findings suggest that patients with PETI should be investigated regardless of the SUV in the presence of other risk factors.

An assessment of our clinical practice in dealing with patient with PETI revealed some trends. In the entire group of 263 patients, the number of patients with diffuse uptake (62%) was much higher than focal uptake (38%). Despite this, the incidence of focal uptake was much higher in patients that underwent further investigation in the form of FNA (73%) or operative intervention (85%). This suggests that the threshold for further investigations is higher in patients with diffuse uptake. Similarly, patients with unilateral uptake are subjected to further investigations more frequently. There were no significant difference in the location of the primary with the majority involving the gastrointestinal tract, breast, lung, and the hematologic system. Although the prevalence of PETI was seen less frequently in patients with primary head and neck malignancies, the prevalence of malignancy was highest in this group.

All the patients in our study with a malignant diagnosis on final histopathology had a primary thyroid malignancy. Although these studies were performed mainly to determine the extent of disease for the primary lesion, the incidence of metastatic involvement of the thyroid is very unlikely. The results of our study suggest that in patients with PETI, the diagnosis is more likely to be a second thyroid primary. This entails that in the presence of risk factors, the investigative algorithm in patients with PETI should be the same as for other patients with isolated thyroid malignancy.

In our present study, 204 patients with PETI did not undergo further investigation for various reasons. In the majority of patients, the extent of disease of the primary did not support any further meaningful investigation of the incidental thyroid lesion. Secondly, since primary thyroid malignancy with its indolent course was the most likely malignant diagnosis in patients with PETI, these patients are more likely to succumb to their primary lesion. Lastly, although patients with diffuse and bilateral uptake comprised the majority of patients, fewer patients in these groups were subjected to further investigations. These findings should be kept in mind when interpreting the results of our study.

In conclusion, in patients undergoing FDG PET scans for evaluation of other primary malignancies, the prevalence of incidentally detected thyroid abnormalities is low. Although the prevalence of FDG PET detected thyroid incidentalomas is low, in patients with such abnormalities, the prevalence of malignancy is high and ranges from 42% to 77%. The factors that significantly correlated with an increased risk of malignancy were the presence of physical finding and focal or unilateral uptake on PET scan. In patients with diffuse uptake or bilateral uptake involving both lobes of the thyroid gland, the prevalence of malignancy is very low. Similarly, the average SUV was not useful in predicting the risk of malignancy. In patients with incidentally detected thyroid abnormalities on PET scan, the presence of certain risk factors such as physical findings in the thyroid gland and focal or unilateral uptake on PET scan warrant further investigation regardless of the SUV within the context of the extent of disease of the primary lesion.


   ACKNOWLEDGMENTS
 
The authors would like to thank Mithat Gonen, PhD, for his assistance in the statistical analysis of this study.

Received for publication May 21, 2006. Accepted for publication May 23, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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