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Original Studies |
Nuclear Medicine and Endocrinology Services, Departments of Radiology, Pathology, and Medicine, The Laurent and Alberta Gerschel Positron Emission Tomography Center, Memorial Sloan-Kettering Cancer Center, New York, New York 10021
Address all correspondence and requests for reprints to: Richard J. Robbins, M.D., Endocrinology Service, Department of Medicine, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, New York 10021. E-mail: robbinsr{at}mskcc.org
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Abstract |
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Recent improvements in clinical assays for serum thyroglobulin (Tg) have improved our ability to detect residual thyroid cancer. However, low iodine-concentrating ability in some tumors may result in the combination of an elevated Tg and a negative DxWBS. Several reviews have recently discussed this clinical dilemma, and some experts advise treatment with high dose 131I to localize and eradicate the metastatic lesions (4). Treatment reduces the Tg level in some cases, but evidence that this treatment approach provides a clinically important benefit is lacking (5).
We examined a newer approach for localizing moderately and poorly differentiated thyroid carcinoma lesions by exploiting the relatively high glucose consumption rate of these malignant cells. Positron emission tomography (PET) using [18F]2-fluoro-2-deoxy-D-glucose (FDG) can localize residual metastatic lesions in thyroid cancer patients with negative DxWBS (6, 7, 8). We performed FDG-PET in a series of 37 patients with negative DxWBS who were being seen for routine thyroid cancer follow-up. All patients had the primary lesions removed surgically, and 33 of them also received 131I ablative therapy before FDG-PET. Eighteen of the subjects had elevated Tg levels. We hypothesized that residual disease in all patients with elevated Tg and negative DxWBS would be localized by FDG-PET.
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Subjects and Methods |
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A total of 96 patients with differentiated thyroid cancer
underwent both FDG-PET and DxWBS over a 3-yr period (from November 1995
to October 1998). In this study, we analyzed only those 37 patients who
had a negative DxWBS (Table 1
). Of these, 23 were female, and 14 were
male. The average age at diagnosis was 47.4 yr, with a minimum of 13 yr
and a maximum of 76 yr. The average age at the time of FDG-PET study
was 54.1 yr, with a minimum of 16 yr and a maximum of 81 yr. The
average interval between diagnosis and FDG-PET was 83.1 months,
with minimum of 2.5 months and a maximum of 456 months.
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All histological diagnoses were made on surgical specimens by attending pathologists at Memorial Sloan-Kettering Cancer Center. All 37 patients had histologically confirmed differentiated thyroid carcinoma. The clinical and pathological staging was performed according to the American Joint Committee on Cancer (AJCC) and represents the highest stage achieved during the patient’s course (9). The patients had following tumor types: 30 papillary, 5 follicular, and 2 Hurthle cell (including 1 case with mixed clear cell) carcinomas. Tumor stage was T1 in 2 cases, T2 in 8 cases, T3 in 1 case, T4 in 22 cases, and Tx in 4 cases. The lymph node status was as follow: 7 patients were node negative (N0), 24 patients were node positive (N1 = 12, N1a = 5, and N1b = 7), and 6 patients had no information concerning lymph nodes metastasis (Nx). Among the 37 patients, 15 patients had distant metastases (M1). The AJCC stages were as follows: 11 stage I, 4 stage II, 10 stage III, and 12 stage IV.
Treatments before FDG-PET evaluation
The patients underwent a variety of initial surgical procedures, including total thyroidectomy in 28 patients, subtotal thyroidectomy in 3 patients, and hemithyroidectomy in 6 patients. Before FDG-PET was performed, 34 of 37 cases had received at least 1 131I treatment (with a range of up to five treatments). The median number of 131I treatments before FDG-PET was 2. The average cumulative dose of 131I before FDG-PET was 11.45 gigabecquerels (309.6 mCi) with a minimum of zero (not including the diagnostic dose) and a maximum of 46.28 gigabecquerels (1251 mCi).
Diagnostic 131I whole body scans
DxWBS was performed as part of the thyroid dosimetry protocol of Benua and Leeper (10, 11). T4 was usually discontinued, and T3 was begun 6 weeks before the commencement of dosimetry. T3 was discontinued 2 weeks before dosimetry. A low iodine diet was initiated 2 weeks before dosimetry and was discontinued only after a decision not to treat the patient or 3 days after 131I treatment. On the initial day of dosimetry, T4, Tg, Tg autoantibody (TgAb), TSH, and serum iodine levels were determined. One patient had dosimetry using recombinant human TSH (rhTSH; Genzyme Transgenics Corp., Cambridge, MA). The procedure was similar, except that the patient continued T4 and received im injections of rhTSH on the 2 days before the dosimetry study (12).
The average diagnostic dose of 131I for DxWBS in the 37 patients was 180.56 megabecquerels (MBq; 4.88 mCi) with a minimum dose of 74.0 MBq (2.0 mCi) and a maximum of 203.5 MBq (5.5 mCi). A high energy and high resolution collimator was used for diagnostic imaging. Anterior and posterior whole body sweep views were obtained at 24, 48, and 72 h, and spot views of the neck and chest were obtained at 2, 4, 24, 48, and 72 h. A lateral view of the neck and chest was obtained at 48 h. In some patients, a delayed 96-h whole body image was also acquired. A negative whole body scan was performed in which no clear focus of abnormal iodine uptake was present by visual inspection, as judged by 2 experienced nuclear medicine physicians.
FDG-PET imaging
All patients underwent FDG-PET imaging after a 6-h fast during which liberal water intake was advised. The study was performed in 21 patients in a high TSH state (including 1 patient with rhTSH) and in 16 patients when TSH levels were low.
PET scans were performed on a General Electric Advance PET scanner (Milwaukee, WI). This camera has a field of view of 55 cm in diameter and 15.2 cm in axial length. Eighteen crystal rings form 35 2-dimensional imaging planes. The system has tungsten septa (1 mm thick and 12 cm long). All scans reported in this study were performed in the 2-dimensional (septa-in) mode. The transaxial resolution is 3.8 mm (FWHM) on the camera central axis, increasing to 7.3 mm at a radial distance of 20 cm. The average axial resolution decreases from 4.0 mm FWHM at the center to 6.6 mm at 20 cm. The total system sensitivity for true events (in kilocounts per s/µCi·cc) is 223, with septa (13). Forty-five to 60 min after the administration of 370 MBq (10 mCi) FDG iv, emission scanning was performed from the level of the maxilla to at least the level of the umbilicus for 6 min at each bed position. A transmission scan was acquired with a 68Ge/68Ga source for attenuation correction for a minimum of 4 min.
Abnormal FDG-PET findings were defined as any focus of increased FDG uptake greater than normal mediastinal activity with SUV maximum levels greater than or equal to 3 (14).
Laboratory criteria
In this cohort, TSH levels were considered low if they fell below 5.0 µIU/dL and high if they were more than 10.0 µIU/dL. Serum Tg was measured by the OptiQuant coated tube immunoradiometric assay (Kronus, San Clemente, CA). All samples were prescreened for the presence of TgAb. This assay is standardized against the BCR Thyroglobulin Reference Preparation RM457. It has a sensitivity of 1 ng/dL and an intraassay coefficient of variation of 2.7% at 5 ng/mL. As there is no universal agreement on specific cut-off levels (15), based on our clinical experience we defined a low thyroglobulin as being less than 2 ng/mL when TSH was suppressed or less than 5 ng/mL when TSH was elevated (16).
Clinical outcomes
As no single test is recognized as a gold standard to indicate the presence or absence of thyroid cancer, the final decision as to the presence or absence of disease took into account all imaging and serological studies and any biopsies that were performed. All patients were cared for in the same medical center by the same team, where multiple imaging studies are performed to assure no evidence of residual disease in each patient. Any iodine-concentrating foci, on DxWBS or RxWBS, were taken as indicating residual disease, as was any elevation of Tg associated with any abnormal imaging study.
Statistical analysis
A 
2 test was used to examine
differences in the lesion detectability of FDG-PET in patients when the
Tg level was elevated compared to when it was low and to determine
whether the TSH status influenced lesion FDG-PET detectability.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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contains a detailed summary
of clinical information for each patient. FDG-PET scans were judged
truly negative (TN) in 13 patients, false negative (FN) in 6, positive
in 14 patients (TP), and false positive (FP) in 4 patients. In the 18
positive FDG-PET patients, limited focal hypermetabolic lesions (4 or
less) were seen in 10 cases; 8 patients had 5 or more abnormal sites
reported as abnormal.
Eighteen patients had an elevated Tg level at the time of FDG-PET,
whereas 19 patients had a low Tg level. There were 12 TP, 1 FP, and 5
FN FDG-PET in the elevated Tg group; there were 2 TP, 13 TN, 1 FN, and
3 FP FDG-PET in the low Tg group (Table 2). The number of abnormal FDG-PET scans
in the elevated Tg group was significantly higher than that in low Tg
group (P < 0.001).
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There were a total of 18 patients in this group. Figure 1 (case 19) details the only case of a
false positive FDG-PET. There were five false negative FDG-PET patients
with elevated Tg. Figure 2 (case 7) had
residual lung metastatic disease on computed tomography (CT) scan with
elevated Tg, but negative DxWBS and FDG-PET scans. Case 18 (Fig. 3) had elevated Tg, a negative DxWBS, and
a false negative FDG-PET. After a therapeutic dose of 131I
(8.51 gigabecquerels; 230 mCi), the RxWBS revealed focal
131I avid uptake in the mediastinum as well as in the
pelvis. The remaining 3 patients with false negative FDG-PET all had
limited regional disease in cervical nodes (cases 5, 15, and 35).
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There were a total of 19 patients in this group. Two of those
patients had true positive FDG-PET. Figure 4 demonstrates a patient (case 31) who
had both negative DxWBS and RxWBS, but FDG-PET revealed a solitary
retrocardiac focus, which was confirmed by chest CT. The nodule was
removed and was found to be metastatic papillary thyroid cancer. Figure 5 illustrates a patient (case 32) with
extensive biopsy-proven lung and bone metastases. Her histological
diagnosis was papillary thyroid cancer with anaplastic components.
There was 1 false negative FDG-PET in the low Tg group (Fig. 6, case 6). There were 3 false positive
FDG-PET in patients with low Tg and negative DxWBS. Two of them proved
to be inflammatory disease. Case 20 had focal inflammation due to a
tracheostomy. A lung biopsy demonstrated granulomatous inflammation in
case 8 (Fig. 7). Case 10 had a solitary
small density in the lung and a borderline positive SUV (3.1) and was
considered to have inflammatory disease by nuclear medicine physicians.
The follow-up CT and CXR showed some resolution by 1 yr.
However, no biopsy was performed on this patient.
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After FDG-PET, 19 of 37 patients had various interventions based on the
FDG-PET results. Five patients underwent surgery for removal of
residual tumor, which resulted in disease-free status in 2 patients,
symptomatic relief in 2 patients (e.g. Fig. 8), and significant tumor debulking in an
additional patient. Four patients underwent biopsies, 13 patients had
131I retreatment (7 were positive on the RxWBS, and 6 were
negative), and 9 patients had repeat DxWBS (all of them were negative).
Three patients were placed on differentiation therapy in an attempt to
stimulate 131I uptake. Table 3 gives a summary of the interventions
and follow-up imaging studies after the initial FDG-PET and the current
disease status for each patient. At the time of publication, 18
patients have no evidence of disease. Isolated elevated Tg exists in 1
patient (case 19) without pathological evidence metastatic of thyroid
cancer. Nine patients have limited disease, and 9 patients have
extensive disease.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The clinical situation of a negative DxWBS in a patient with prior metastatic disease could represent a cure, microscopic residual disease, or a loss of iodine-transporting ability in macroscopic residual tumor. The concomitant elevation of serum Tg is usually taken as evidence of residual disease. The use of FDG in such patients has only been reported as part of several larger series (19, 20, 24). We hypothesized that FDG-PET would localize residual disease in all patients with elevated serum Tg levels and negative DxWBS. The disease was localized in 12 of 18 such patients, but 5 patients had false negative scans. We were unable to locate the disease on any imaging modality in 1 patient. It is important to discuss the false results in some detail to refine the clinical usefulness of this new technology for identifying metastatic thyroid cancer.
Summary of FDG-PET results
We examined 37 patients who had negative DxWBS. The FDG-PET scans were positive in 49% of the patients. In the 18 patients who also had elevated Tg levels, 71% had a positive FDG-PET. Of 19 patients with low Tg levels, only 26% had a positive FDG-PET. As 3 of these were false positives (e.g. inflammation), the true FDG-PET positivity was only 10% in patients with low Tg. For the entire group, FDG-PET had a sensitivity of 70% and a specificity of 76.5%.
FDG-PET findings in the elevated Tg group
In the 18 patients with elevated Tg levels, 17 had clear evidence of residual thyroid cancer. FDG-PET accurately localized the disease in 12 of these patients. Three patients had minimal disease in cervical nodes, detected by ultrasonography. They are categorized as false negatives because FDG-PET did not localize the disease. Our results differ therefore from a report that FDG-PET was useful in detecting small malignant lymph nodes (24). Brandt-Mainz et al. (25) reported 3 of 20 patients with false negative FDG-PET who had cervical nodes detected by ultrasonography. Although the size of the node is a factor, the uptake and retention of FDG may be more important. Well differentiated cells may have relatively low FDG uptake, and this combined with minimal tumor volume can lead to false negative scans. Therefore, a negative FDG-PET does not exclude residual thyroid cancer in cervical lymph nodes.
Only one patient (case 18) clearly had distant metastases that were not seen on FDG-PET. It is likely that the 5 mCi 131I given for the diagnostic scan was insufficient to localize the small differentiated metastatic lesions, which were seen on RxWBS after a high dose 131I treatment. One patient (case 19) was categorized as a false positive because the only region identified by FDG-PET (the humerus) was shown to be fibrous dysplasia on biopsy. However, this case is difficult to categorize, as he also had an elevated Tg level and a paratracheal mass, suggestive of but not proven to be thyroid cancer.
The sensitivity of FDG-PET in our DxWBS-negative patients with elevated Tg levels is therefore 71% (12 of 17); the specificity is not calculable as the only high Tg patient without disease had a false positive FDG-PET. This compares to the 82% sensitivity level reported by Dietlein (24) in a smaller series, to the 100% sensitivity reported by Grunwald in 5 patients with elevated Tg levels (19), and to the 72% sensitivity in similar patients reported by Brandt-Mainz and co-workers (25). Altenvoerde et al. (20) recently reported FDG-PET results in a group of 9 patients with negative DxWBS and elevated Tg levels. Unfortunately, specificity and sensitivity could not be calculated unambiguously from this report.
FDG-PET findings in the low Tg group
Of the 19 patients with low Tg levels, 13 were believed to have no evidence of disease (true negatives). Three individuals had focal uptake of FDG that proved not to be thyroid cancer on subsequent biopsy and long term follow-up with other image modalities. The findings in our patients with low Tg suggest that inflammatory diseases are not an uncommon explanation for a positive FDG-PET (19, 23, 24).
One patient in the low Tg group had a false negative scan. She was subsequently shown to have abnormal cervical lymphadenopathy as well as TgAb, which may have artifactually lowered the Tg level. The presence of low Tg levels in patients with metastatic thyroid cancer is well described (26) and may be a major problem in previous reports, as assay interference caused by TgAb was not always recognized.
Therefore, in our low Tg group, FDG-PET had a sensitivity of 67% (2 of 3) and a specificity of 81% (13 of 16). Altenvoerde et al. (20) reported that all 3 patients with negative DxWBS and low Tg levels had negative FDG-PET and no evidence of cancer. Grunwald et al. (19) reported negative FDG-PET in 8 of 9 patients with negative DxWBS and low Tg levels for a specificity of 89%, very similar to our experience.
Correlation between stage and FDG-PET positivity
The clinical stage of the disease, as based on the AJCC staging system, was examined as a predictor of FDG-PET outcome. Patients who had negative DxWBS and were stage I had no positive FDG-PET (11 of 11), although 2 with elevated Tg levels had minimal disease. All stage I patients with low Tg levels were judged to have no evidence of disease by FDG-PET. FDG-PET was positive in 25% of stage II, 60% of stage III, and 84% of stage IV patients. Of the 10 stage IV patients with elevated Tg levels, all had disease localized by FDG-PET. Therefore, FDG-PET are generally not necessary in stage I patients with low Tg and can be expected to have a very low yield of true positive findings in such patients. Conversely, FDG-PET always localized disease in stage IV patients with high Tg levels. This was useful in determining whether the metastatic lesions were present in critical locations (e.g. in the brain or spinal cord) that needed additional therapeutic measures.
Clinical impact of FDG-PET
One of the factors in determining the value of a new diagnostic approach is to assess its impact on patient management. In this regard, we analyzed each case and interviewed the clinicians involved. The FDG-PET result had a definite impact on patient management in 19 of the 37 patients, or more than half. In 13 cases, the patients were given high doses of 131I despite prior negative DxWBS. Seven of these patients showed 131I retention in metastatic lesions on RxWBS. Unfortunately, the FDG-PET result was unable to predict which patients would concentrate radioiodine. In 9 cases, an additional surgical procedure was performed to identity the nature of the FDG-PET findings or to resect disease that was threatening a critical organ. Three patients were started on differentiation therapy with retinoic acid after FDG-PET.
Does TSH influence FDG-PET results?
In normal thyroid cells, TSH stimulates cellular metabolism and raises the glucose consumption rate by altering glucose transporter expression (27). Sisson found higher FDG uptake in a lung lesion when the patient was hypothyroid (8). By comparing scan outcomes in patients with low and high TSH levels, we attempted to explore this phenomenon in human thyroid cancer cells in vivo. We found no statistical difference among the four different outcomes (TP, TN, FP, FN) when the high TSH group was compared to the low TSH group. Furthermore, four patients in this group underwent FDG-PET when TSH levels were high and again when they were low. The SUV levels were slightly higher in some lesions when the TSH was elevated; however, this difference had no clinically significant effect on scan interpretation and did not alter the diagnosis or management.
In this study, we did not compare the sensitivity or specificity of FDG-PET with those of other imaging agents that have been used in thyroid cancer. Agents that have been used to localize metastatic lesions in thyroid cancer include 201thallium (201Tl), 99mTc-furifosmin, and 99Tc-methoxyisobutylisonitrile. Recent studies have found that FDG-PET has better sensitivity and resolution than 201Tl (28), 99mTc-furifosmin (25), or 99Tc-methoxyisobutylisonitrile (19, 23, 29). It is important to point out that these agents are more widely available and less expensive than FDG-PET.
In summary, we found that FDG-PET localized residual disease in 71% of thyroid cancer patients who had negative DxWBS and elevated serum TG. It had a 92% positive predictive value when Tg was elevated, and a 93% negative predictive value when Tg was not elevated. The FDG-PET outcome could be predicted in stage I patients (always negative) and in stage IV patients with elevated Tg levels (always positive). However, in this later group there is not as much uncertainty about the presence of residual disease, but there is more concern about the location of specific lesions. This ability to precisely localize the viable disease led to changes in patient management in over half of the patients. Four of the six false negatives in this study were due to patients with a small amount of differentiated thyroid cancer in neck nodes and to falsely low Tg levels, often caused by Tg autoantibodies. It is important to emphasize that FDG-PET is not a good test to detect residual cervical lymph nodes. Three of the four false positive FDG-PET results in this study were due to inflammatory diseases. In conclusion, FDG-PET is an effective way to localize residual disease in thyroid cancer patients who have negative DxWBS and elevated Tg.
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Acknowledgments |
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Received November 10, 1998.
Revised December 22, 1998.
Accepted March 30, 1999.
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References |
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H. A. Macapinlac Clinical Usefulness of FDG PET in Differentiated Thyroid Cancer J. Nucl. Med., January 1, 2001; 42(1): 77 - 78. [Full Text] [PDF]
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F. Grunwald and H.-J. Biersack FDG PET in Thyroid Cancer: Thyroxine or Not? J. Nucl. Med., December 1, 2000; 41(12): 1996 - 1998. [Full Text] [PDF]
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M. van Tol, P. L. Jager, R. P. F. Dullaart, and T. P. Links Follow-Up in Patients with Differentiated Thyroid Carcinoma with Positive 18F-Fluoro-2-Deoxy- D-Glucose-Positron Emission Tomography Results, Elevated Thyroglobulin Levels, and Negative High-Dose 131I Posttreatment Whole Body Scans J. Clin. Endocrinol. Metab., May 1, 2000; 85(5): 2082a - 2083. [Full Text]
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W. Wang, S. M. Larson, M. Fazzari, S. K. Tickoo, K. Kolbert, G. Sgouros, H. Yeung, H. Macapinlac, J. Rosai, and R. J. Robbins Prognostic Value of [18F]Fluorodeoxyglucose Positron Emission Tomographic Scanning in Patients with Thyroid Cancer J. Clin. Endocrinol. Metab., March 1, 2000; 85(3): 1107 - 1113. [Abstract] [Full Text]
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