Thyroid Ablation with 1.1 GBq (30 mCi) Iodine-131 in Patients with Papillary Thyroid Carcinoma at Intermediate Risk for Recurrence

Abstract

Background:

Little is known about the medium- and long-term outcomes of thyroid ablation with 1.1 GBq (30 mCi) ¹³¹I in patients with papillary thyroid carcinoma who have a tumor >4 cm or accompanied by extrathyroid invasion or clinically detected lymph node metastases (cN1). The objective of this study was to evaluate the efficacy of ablation with 30 mCi ¹³¹I in this subgroup of patients and to report the medium-term outcomes.

Methods:

We studied 152 patients with papillary thyroid carcinoma submitted to total thyroidectomy with apparently complete tumor resection, who had a tumor >4 cm or 2–4 cm accompanied by extrathyroid invasion or lymph node metastases, or ≤2 cm accompanied by both extrathyroid invasion and lymph node metastases. Patients with extensive extrathyroid invasion by the primary tumor were excluded. Lymph node involvement was detected by ultrasonography or palpation (cN1).

Results:

Forty-two patients were prepared by administration of recombinant human thyrotropin and 110 by levothyroxine withdrawal. Posttherapy whole-body scanning revealed unequivocal ectopic uptake in three patients. When evaluated 9–12 months after ablation, 123 patients had achieved complete ablation (stimulated thyroglobulin [Tg] <1 ng/mL, negative anti-Tg antibodies, and neck ultrasonography); a new posttherapy whole-body scanning revealed persistent disease in 2 patients whose initial posttherapy whole-body scanning (obtained at the time of ablation) had already shown ectopic uptake; 12 patients presented with a Tg >1 ng/mL and 14 had positive anti-Tg antibodies without apparent metastases; 1 patient had metastases not detected at the time of ablation. Recurrence was observed in an additional 6 patients during follow-up (median 76 months). There was no case of death related to the disease. Therefore, an activity of 30 mCi failed in only 9 (6%) patients with persistent disease or recurrence after ablation. None of the variables analyzed (sex, age, tumor size, multicentricity, extrathyroid invasion, lymph node metastases, preparation [recombinant human thyrotropin or levothyroxine withdrawal]) was a predictor of ablation failure.

Conclusions:

An activity of 30 mCi ¹³¹I is effective in thyroid ablation in patients with stage T3 and/or N1papillary thyroid carcinoma.

Introduction

Radioactive iodine is indicated after thyroidectomy in many patients with papillary thyroid carcinoma (PTC). A high activity of ¹³¹I is recommended when tumor resection is incomplete, clinically or radiologically apparent metastases persist after surgical treatment, and in the case of extensive extrathyroid invasion by the primary tumor or very significant lymph node involvement (1 –8). In the remaining patients, the ¹³¹I activity for ablation is controversial. In comparison to an activity of 3.7 GBq (100 mCi) ¹³¹I, the advantages of an activity of 1.1 GBq (30 mCi) include lower radiotoxicity (9,10) and no requirement of hospitalization.

Current guidelines still contain restrictions regarding the use of an activity of 30 mCi ¹³¹I for thyroid ablation. Some guidelines recommend higher activities for all patients with PTC (2,4,11), whereas others do not indicate 30 mCi when the tumor is larger than 4 cm (1,3,5,7,8). An activity of 30 mCi ¹³¹I is also not recommended (1,3,7), or is not the first choice (5,6,8), in the case of tumors with extrathyroid invasion or lymph node metastases detected by ultrasonography (US) or palpation (cN1), especially in the presence of both, or when the primary tumor is larger than 2 cm.

Although there are a number of reports evaluating the efficacy of 30 mCi ¹³¹I for thyroid ablation, only few studies included a significant number of patients with large or invasive tumors or with clinically detected lymph node metastases (cN1) and reported the medium- and long-term outcomes in this subgroup (12 –14). In the ESTIMABL study (15), none of the participants had a tumor >4 cm or an invasive (T3) tumor, and less than 20% had lymph node metastases (N1), all with tumors ≤2 cm (T1N1). In the HiLo study (16), less than one-fourth of patients had a tumor >4 cm or an invasive (T3) tumor, and only about 15% had lymph node metastases (N1), with <5% being stage T3N1. The medium- and long-term outcomes of these two large studies (15,16) are not yet available.

These data highlight the importance of further studies reporting the medium- and long-term outcomes of thyroid ablation with 30 mCi ¹³¹I in this subgroup of patients with PTC who are at high (1,3,4,17) or intermediate (5,6) risk for recurrence, which is the obective of this study.

Patients and Methods

Patients

All patients with PTC seen by the first author (P.W.R.) between 2001 and 2011, who had received 30 mCi ¹³¹I after total thyroidectomy, met the following criteria: (i) apparently complete tumor resection; (ii) no metastases detected by clinical examination, simple chest X-ray, or neck US performed after surgery and before ablation; (iii) no extensive extrathyroid invasion (pT4). Patients with the following characteristics were selected for this study: (i) tumor >4 cm with or without extrathyroid extension, or (ii) tumor measuring 2–4 cm accompanied by extrathyroid invasion and/or lymph node metastases (cN1), or (iii) tumor ≤2 cm accompanied by both extrathyroid invasion and lymph node metastases (cN1). Since none of the patients was submitted to elective dissection, lymph node involvement was suspected by palpation or US (cN1) in all of them.

Ablation with ¹³¹I

Approximately 3–6 months after thyroidectomy, the patients were submitted to ablation with ¹³¹I after levothyroxine (L-T4) withdrawal for 4 weeks or administration of recombinant human thyrotropin (rhTSH) and administration of a low-iodine diet for 10 days before the procedure. Anterior and posterior whole-body images were obtained seven days after ablation with ¹³¹I (posttherapy whole-body scanning [RxWBS]).

Initial assessment after ablation

The patients were evaluated 9–12 months after ablation by the measurement of thyroglobulin (Tg) on L-T4 (Tg/T4) and anti-Tg antibodies (TgAb), and by neck US. Other imaging methods (chest and mediastinal computed tomography [CT], whole-body scanning with ^99mTc-sestamibi, fluorodeoxyglucose–positron emission tomography [FDG-PET]/CT) were performed in patients with negative US and Tg/T4 >1 ng/mL. A stimulated Tg was measured in patients with Tg/T4 <1 ng/mL and negative US. Ablation was considered to be complete when the stimulated Tg continued to be <1 ng/mL in the absence of circulating TgAb. Other imaging methods were also performed in patients with Tg/T4 <1 ng/mL and Tg >10 ng/mL after L-T4 withdrawal or >5 ng/mL after rhTSH (6,18 –22), or with stimulated Tg >1 ng/mL in the presence of circulating TgAb (23).

Late follow-up

Patients without apparent disease in the initial assessment were followed up by annual measurement of Tg/T4 and TgAb, and by neck US. Patients with initial Tg/T4 levels <1 ng/mL, but with a stimulated Tg >1 ng/mL, were submitted to repeated Tg stimulation at an interval of 2 years (24) until the stimulated Tg became <1 ng/mL.

Imaging methods other than US (chest and mediastinal CT, ^99mTc-sestamibi scans, FDG-PET/CT, and RxWBS after an empirical activity of 3.7 GBq ¹³¹I) were performed if (i) Tg/T4 <1 ng/mL converted to levels >1 ng/mL; (ii) Tg elevation (Tg/T4 or stimulated Tg) >50% when Tg was already >1 ng/mL (24 –26); (iii) negative TgAb became positive; or (iv) TgAb titers further increased when they were already positive.

Patients without apparent disease who had a stimulated Tg <1 ng/mL and negative TgAb were maintained on an L-T4 dose sufficient to obtain serum TSH levels of 0.1–0.5 mIU/L. Patients with elevated Tg or positive TgAb were maintained on an L-T4 dose sufficient to obtain serum TSH levels ≤0.1 mIU/L as long as these markers continued to be elevated.

The time of follow-up ranged from 18 to 140 months (median 76 months). Apparent disease was defined based on the results of the imaging methods, cytology or histology, and/or unequivocal ectopic uptake (excluding false-positive results) on RxWBS or FDG-PET.

The study was approved by the Research Ethics Committee of our Institution and all subjects gave written informed consent.

Assays

Until 2006, Tg was measured by a radioimmunometric assay (ELSA-hTG; CIS Bio International) with a functional sensitivity of 1 ng/mL. After 2006, Tg was measured by a chemiluminescent assay (Access Thyroglobulin Assay; Beckman Coulter) with a functional sensitivity of 0.1 ng/mL. TgAb was measured by a chemiluminescent assay (Immulite 2000 [Diagnostic Products Corporation; reference value of up to 40 IU/mL] or ARCHITET Anti-Tg [Abbott Laboratories; reference value of up to 4.11 IU/mL]).

Imaging methods

US was performed with a linear multifrequency 12–14 MHz transducer for morphological analysis (B-mode) and for power Doppler evaluation. US was defined as negative when no suspicious lesions were detected (27) or, in the presence of these lesions, when cytology and Tg measurement in the needle washout fluid obtained by US-guided fine-needle aspiration were negative.

Chest and mediastinal CT was performed on 5 mm sequential sections. ^99mTc-sestamibi scans were performed under L-T4 therapy using a tracer dose of 720–925 MBq. Whole-body images were obtained early (20 minutes) and late (6 hours). FDG-PET/CT was carried out after stimulation with rhTSH or L-T4 withdrawal for 4 weeks according to a recommended protocol (28).

Statistical analysis

The Fisher exact test or the χ ²-test was used to detect differences in the proportion of cases. Multivariate Cox regression models were used to assess the independent effect of different variables on the risk for persistent or recurrent disease. A p-value <0.05 was considered to be significant.

Results

Characteristics of the patients

A total of 152 patients were studied and their characteristics are shown in Table 1. According to the risk stratification of the European Thyroid Association (1), French Society of Endocrinology (3), Latin American Thyroid Society (4), and European Society for Medical Oncology (17), all patients were classified as high risk. The classification of the Brazilian Society of Endocrinology and Metabolism (5) classified all patients as intermediate risk. According to the classification proposed by the American Thyroid Association (6), 12% were at low risk (tumor >4 cm) and 88% were at intermediate risk. According to the American Joint Committee on Cancer (6), 52.6% of the patients were at high risk for mortality (stage III or IVA [age >45 years, pT3 and/or cN1]).

Table 1.

Characteristics of the Patients Studied

Sex
Female	111 (73%)
Male	41 (27%)
Age (years)	12–80 (mean 48.5)
Family history of thyroid cancer	11 (7%)
History of radiation exposure	1 (0.65%)
Tumor size
Range	0.8–5.5 cm
≤1 cm	3 (2%)
>1 cm and ≤2 cm	11 (7%)
>2 cm and ≤4 cm	98 (64.5%)
>4 cm	40 (26.3%)
Histological subtype
Classic	110 (72.3%)
Follicular variant (nonencapsulated)	24 (15.8%)
Diffuse sclerosing	10 (6.5%)
Oxyphilic cells	8 (5.2%)
Multicentricity of the tumor	47 (31%)
Minimal extrathyroid invasion	92 (60.5%)
Lymph nodes metastases (cN1)
Number of patients	84 (55%)
Positive preoperative US	50^a
Negative US/positive perioperative evaluation	35^b
Central and lateral metastases	43
Only central metastases	39
Only lateral metastases	3
N1a	39
N1b	46
TNM classification (6)
T2N1	30 (20%)
T3N0	68 (44.5%)
T3N1	54 (35.5%)

Lymph nodes seen only in the lateral compartments (n=36), in lateral and central compartments (n=10), and only in the central compartment (n=4).

Lymph nodes detected in the central compartment.

US, ultrasonography.

Ablation with ¹³¹I

Forty-two patients were prepared by administration of rhTSH and 110 by L-T4 withdrawal. These groups were similar in terms of sex, age, tumor size, multicentricity, extrathyroid invasion, lymph node metastases, TNM stage, risk category (6), and frequency of ectopic uptake on RxWBS. RxWBS showed unequivocal ectopic uptake in three patients (cervical, mediastinal, and pulmonary) and a doubtful result regarding the metastatic nature in two patients (cervical in both).

Initial assessment after ablation

When evaluated 9–12 months after ablation, 123 patients had achieved complete ablation (stimulated Tg <1 ng/mL, negative TgAb and neck US); a new RxWBS scan revealed persistent disease in two patients whose initial RxWBS (obtained at the time of ablation) had already shown ectopic uptake (mediastinal in one and pulmonary in one); 12 patients presented with a Tg >1 ng/mL and 14 had positive TgAb in the absence of apparent disease detected by imaging methods; US detected cervical lymph node metastases (not detected at the time of ablation) in one patient.

Late follow-up

During follow-up, 6/149 (4%) patients without apparent disease in the initial assessment presented recurrence, including lymph node metastases in 5 (detected by US in 4 and by FDG-PET/CT in 1) and pulmonary metastases in 1 (detected by a new RxWBS scan). Tumor recurrence was observed in 2/123 (1.6%) patients who achieved complete ablation and in 4/26 (15.4%) in whom elevated Tg or TgAb persisted in the first year after ablation.

The 143 patients without persistent or recurrent disease were not submitted to any additional therapy. Of these, 115 had undetectable Tg/T4 (0.1 ng/mL) and negative TgAb in the last assessment. Eighteen patients had detectable Tg/T4 ≤0.27 ng/mL (29) at stable or declining concentrations. Tg/T4 >0.27 ng/mL persisted in 5 patients (0.41, 0.52, 0.56, 1.05, and 1.8 ng/mL, respectively) and positive TgAb persisted in the other 5. A decrease in the concentration of these markers was observed in all of these patients.

In the last assessment, four of the nine patients with persistent or recurrent disease achieved remission after surgical treatment and/or radioactive iodine therapy. Two patients continued to present elevated but declining Tg levels in the absence of apparent metastases, and metastases were still detected by the imaging methods in the other two.

There was no case of death related to the disease.

Factors predicting ablation failure

Considering the 2 patients with a positive initial RxWBS, in whom apparent disease persisted 9–12 months after ablation, and the 7 patients with negative initial RxWBS and subsequent recurrence, ablation with 30 mCi failed in only 6% of cases. None of the variables analyzed (sex, age, tumor size, multicentricity, extrathyroid invasion, lymph node metastases [presence and number], preparation [rhTSH or L-T4 withdrawal]) was a predictor of ablation failure.

Discussion

First, to our knowledge, this is the largest study evaluating the medium-term outcomes of thyroid ablation with 30 mCi ¹³¹I in patients with PTC >4 cm or with extrathyroid invasion and/or clinically detected lymph node metastases (cN1). Second, the follow-up protocol of the patients (including imaging methods) is in accordance with current guidelines. In fact, it is possible that the recurrence rates reported in older studies are underestimated as a result of the use of less sensitive methods such as diagnostic WBS and simple chest X-ray rather than US, CT, and, more recently, FDG-PET/CT. Third, although further recurrences are possible, we do not believe that they will occur in a sufficient number to significantly alter the rate observed. It is known that approximately 80% of tumor recurrences are diagnosed in the first 5 years of follow-up (30). At the end of the study, only 10 patients had a Tg/T4 >0.27 ng/mL (29) or positive TgAb. Moreover, a reduction of Tg and TgAb concentrations, a known predictor of disease-free survival (24,25,31,32), was observed in all of these patients.

Studies using older follow-up protocols already demonstrated the efficacy of an activity of 30 mCi in patients with PTC and extrathyroid invasion or lymph node metastases (12,33,34). Using an updated protocol, two recent series also reported the medium- and long-term outcomes of ablation with a low ¹³¹I activity in intermediate-risk patients (13,14). In the series of Molinaro et al. (13), additional treatment (after ablation) was necessary in 18/55 patients (32.7%) with stage II or III tumors [DeGroot classification (35)] after 10 years of follow-up. Similar findings were reported by Castagna et al. (14) for 23/85 patients (27%) at intermediate risk [ATA classification (6)] after a median follow-up period of 4.2 years. It should be noted that, in contrast to the present series, many patients received additional treatment with ¹³¹I because of an elevated Tg, but with negative imaging scans, especially in the first study (13). Neck US was not performed before ablation in those series (13,14). It is therefore possible that some of the lymph node metastases detected after ablation were already present on that occasion. In contrast, we routinely perform US before ablation and exclude patients with persistent metastases after thyroidectomy. These factors explain, at least in part, the higher failure rates reported in those series (13,14) when compared with the present one. The frequency of additional treatment did not differ significantly between patients in stages II and III versus stage I in the study of Molinaro et al. (13), or between patients receiving low versus high ¹³¹I activities in the study of Castagna et al. (14). Finally, although not reporting results on medium- and long-term recurrence, other recent studies also demonstrated the efficacy of thyroid ablation with 30 mCi ¹³¹I in patients with stage T3 and/or N1 tumors (16,36).

Recombinant human TSH is currently the preparation of choice for thyroid ablation. In the present series, ablation with 30 mCi ¹³¹I showed equal medium-term (median 76 months) efficacy when preceded by rhTSH or L-T4 withdrawal, even in the case of intermediate-risk patients. Specifically in this subgroup of patients (large tumors or accompanied by extrathyroid invasion and/or lymph node metastases), previous studies have shown a similar short-term (16,36) and medium- and long-term (13,14) efficacy of rhTSH and hypothyroidism for ablation with 30 mCi ¹³¹I.

We conclude that thyroid ablation with 30 mCi ¹³¹I and rhTSH is effective even in patients with tumors >4 cm or accompanied by minimal extrathyroid invasion and/or lymph node metastases, but with apparently complete tumor resection.

Footnotes

Author Disclosure Statement

The authors declare that no competing financial interests exist.

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Thyroid Ablation with 1.1 GBq (30 mCi) Iodine-131 in Patients with Papillary Thyroid Carcinoma at Intermediate Risk for Recurrence

Abstract

Background:

Methods:

Results:

Conclusions:

Introduction

Patients and Methods

Patients

Ablation with 131I

Initial assessment after ablation

Late follow-up

Assays

Imaging methods

Statistical analysis

Results

Characteristics of the patients

Ablation with 131I

Initial assessment after ablation

Late follow-up

Factors predicting ablation failure

Discussion

Footnotes

Author Disclosure Statement

References

Ablation with ¹³¹I

Ablation with ¹³¹I