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Combination of Radioiodine (¹³¹I) and Probe-Guided Surgery for Persistent or Recurrent Thyroid Carcinoma

Institut Gustave-Roussy, 94 805 Villejuif Cedex, France

Address all correspondence and requests for reprints to: M. Schlumberger, M.D., Service de Médecine Nucléaire, Institut Gustave-Roussy, 39 rue C. Desmoulins, 94805 Villejuif Cedex, France.

	Abstract

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To improve the completeness of surgical excision of persistent or recurrent differentiated thyroid carcinoma, the following protocol was used for the treatment of 54 patients with functioning lymph node metastases: administration of 3.7 gigabecquerels (100 mCi) ¹³¹I; total body scintigraphy (TBS) on day 4; surgery on day 5, using an intraoperative probe (Gammed 2, Eurorad); and postoperative TBS with the remaining ¹³¹I activity on day 7.

The 54 patients (35 women and 19 men presenting 47 papillary carcinomas, 2 well differentiated follicular carcinomas, and 5 poorly differentiated follicular carcinomas) had already undergone surgery for differentiated thyroid carcinoma: total thyroidectomy (51 patients) or lobectomy with isthmusectomy (3 patients), with lymph node dissection in 33. One to 7 ¹³¹I treatments were performed before inclusion.

Preoperative ¹³¹I-TBS with a high dose of ¹³¹I allowed accurate localization of previously suspected neoplastic foci and detection of yet unknown foci in 56%; it was the most sensitive tool for localizing neoplastic foci. The use of an intraoperative probe was considered decisive in 20 patients, as neoplastic foci were found inside sclerosis due to previous surgery (n = 9), at unusual sites behind vessels or in the mediastinum (n = 10), or both (n = 1). In 26 patients, it facilitated the preoperative detection of foci with ¹³¹I uptake already depicted at preoperative ¹³¹I-TBS. In all 46 patients, the completeness of excision was demonstrated by both the probe and the postoperative ¹³¹I-TBS and was confirmed during follow-up. Of note, lymph node metastases undetected by ¹³¹I-TBS or by the probe were found in 14 patients at histological examination. This clearly shows that en block dissection is the only recommended procedure.

In four patients, no neoplastic foci were found and in four patients, uptake was either due to the thymus (in two) or to the salivary glands (in two).

	Introduction

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LYMPH node involvement, a frequent feature in differentiated thyroid carcinoma, is observed in 15–60% of papillary and 10–40% of follicular carcinomas (1, 2). Extensive lymph node involvement is associated with a high risk of local recurrence (1, 3, 4, 5) and lung metastases (6) and in only a few studies with a reduced survival rate (4, 7, 8).

The role of surgery in the treatment of persistent or recurrent lymph node metastases from differentiated thyroid carcinoma is still debated. Radioiodine (¹³¹I) alone can effectively treat tumor foci exhibiting radioiodine uptake as long as a radiation dose of at least 8000 cGy can be delivered, whereas response is virtually nonexistent for doses below 3500 cGy (9). Response to ¹³¹I is also better in tumor foci that are smaller than 1 cm in diameter. Indeed, ¹³¹I uptake was still detectable after three ¹³¹I treatment doses in only 24% of patients who then underwent surgery (10). In contrast, treatment with ¹³¹I is less efficient in patients with larger tumor deposits (11, 12, 13); ¹³¹I uptake was still detectable after repeated ¹³¹I treatments in 80% of these cases (1, 10, 14). Even when lymph node metastases cease to concentrate ¹³¹I, they may continue to be palpable or detectable at ultrasonography. Histological examination of lymph nodes confirmed the persistence of neoplastic cells likely to cause late relapses in comparable cases (5). This constitutes the basis for surgical excision of lymph node metastases even if they are able to concentrate ¹³¹I.

However, when performed, surgery should be complete and accomplished in a single procedure. An accurate preoperative work-up indicating the lymph node areas to be dissected is mandatory. Imaging modalities, including ultrasonography, computed tomography (CT) scan, and magnetic resonance imaging are sensitive but may be difficult to interpret in previously dissected areas. In contrast, total body scan with ¹³¹I (¹³¹I-TBS) may demonstrate neoplastic foci with a high specificity. Furthermore, reports have indicated that posttherapy ¹³¹I scan may detect new lesions in up to 50% of patients and is the most sensitive tool in patients with functioning metastases (15, 16, 17, 18, 19). An intraoperative probe can be useful for tumors targeted by a specific radioactive tracer (20, 21); this is particularly relevant in differentiated thyroid carcinoma patients with lymph node metastases when they are either in unusual locations or embedded in sclerosis resulting from previous surgery.

In this study, 54 consecutive patients with persistent or recurrent disease in the neck and/or the mediastinum with ¹³¹I uptake were enrolled in the following protocol: preoperative administration of a high dose [3.7 gigabecquerels (GBq)/100 mCi] of ¹³¹I, yielding a sensitive TBS 4–5 days later, followed by surgery using an intraoperative probe, and another TBS with the remaining ¹³¹I activity 2 days after surgery.

	Subjects and Methods

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Patients

Fifty-four patients who had already undergone surgery for thyroid carcinoma were included in the present study between 1988 and 1996. There were 35 female and 19 male patients, ranging in age from 7–63 yr at the time of initial treatment. The time elapsed from initial surgery to inclusion in the study ranged from 5 months to 29 yr (mean, 5 yr). Forty-seven patients had papillary thyroid carcinoma, 2 had minimally invasive follicular cancer, and 5 had widely invasive, poorly differentiated thyroid carcinoma. Thyroid carcinoma was aggressive in most patients, as shown by extracapsular involvement in 86%, vascular invasion in 33%, multifocality in 75%, and bilaterality in 47% of cases. Lymph node metastases were found in 71% at initial surgery.

Initial surgery included total (or near-total) thyroidectomy in 51 patients and lobectomy with isthmusectomy in 3; dissection of various lymph node areas was performed in 33 patients (Table 1). Differences in the extent of surgery among patients stemmed from the fact that most of them had undergone initial surgery in various centers and had been referred to the Institut Gustave-Roussy for the treatment of persistent or recurrent disease. After initial surgery, all patients had been treated with 3.7 GBq (100 mCi) ¹³¹I; the number of ¹³¹I treatments ranged from 1–7 before inclusion in the study.

Before treatment in this study, 10 patients had unilateral vocal cord paralysis and 7 had hypoparathyroidism.

This study was performed in accordance with the ethical rules of our institution.

Methods

All patients underwent a clinical examination. Neck ultrasonography was performed in 20 patients using an 8-MHz linear probe (Eccocee, Toshiba, Tokyo, Japan). Twenty-seven patients had a CT scan of the neck and chest, with injection of contrast medium, more than 6 weeks before the administration of ¹³¹I. The first 18 patients included in the study had total body scintigraphy with 74–185 megabecquerels (MBq; 2–5 mCi). Thereafter, a high dose of ¹³¹I (3.7 GBq/100 mCi) was administered without performing any previous ¹³¹I-TBS with a diagnostic dose. Serum thyroglobulin (Tg) levels were measured using a commercial kit, with a sensitivity of 1 ng/mL (Dynotest Tg, Brams, Berlin, Germany). Two patients with serum interference in the assay were excluded from Tg determination.

Patients received 3.7 GBq (100 mCi) ¹³¹I on day 0. T₄ treatment was withdrawn for 5 weeks and T₃ was withdrawn for 2 weeks before ¹³¹I administration. At that time, the serum TSH level was above 30 µU/mL in all patients. A total body scan was performed using a double head whole body scintiscanner or a double head -camera equipped with high energy collimators on day 4. A neck scintigraphy was also performed in each patient using a rectilinear scintiscanner for precise anatomical localization of each focus of uptake (Fig. 1).

View larger version (69K): [in this window] [in a new window]   Figure 1. Preoperative and postoperative 131I neck scintigraphy examples. a, Preoperative neck scintigraphy, 4 days after 3.7 GBq 131I, showing paratracheal and jugulo-carotid foci of uptake. b, Postoperative neck scintigraphy of the same patient, with the remaining activity of 131I, showing the disappearance of all foci of uptake.

For radioprotection studies, the radiation dose received by the surgeon during surgery was evaluated by dosimeters, using high sensitivity thermoluminescent equipment (Fimel, Paris, France). Six dosimeters were taped onto the surgeon’s finger tips: the thumb, middle, and ring fingers of right and left hands; one on his neck; and one on his forehead. Also, a portable, dedicated device was used to measure radioactive contamination on surfaces and surgical tools after surgery; all measurements were negative.

A postoperative total body scan was performed on day 7 with the remaining ¹³¹I activity. Patients were then followed up with Tg and TSH measurements 3–6 months later during L-T₄ treatment and with a TBS using 74–185 MBq (2–5 mCi) or 3.7 GBq (100 mCi) ¹³¹I and with Tg measurements off L-T₄ treatment, 1 yr later.

	Results

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Preoperative work-up

In 22 patients (38%), lymph nodes were palpable in the jugulo-carotid chains. Neck ultrasonography, performed in 20 patients, showed abnormalities in 19 corresponding to foci of uptake on ¹³¹I-TBS. Among the 27 patients who underwent CT scan of the neck and chest, lymph nodes were larger in the mediastinum than initially suspected on ¹³¹I-TBS in 2 patients, and CT scan studies showed lesions similar to those found on the ¹³¹I-TBS in 8 patients. In the other patients, CT scan was either normal (n = 8) or doubtful due to previous surgery (n = 9).

Eighteen patients had a ¹³¹I-TBS with both 74–185 MBq (2–5 mCi) and 3.7 GBq (100 mCi), and in 10 (56%), the high dose ¹³¹I-TBS depicted foci of uptake that were not suspected with 74–185 MBq. Due to this higher sensitivity, only the high dose ¹³¹I-TBS (3.7 GBq) was performed in subsequent patients, and the 74–185 MBq ¹³¹I-TBS was henceforth omitted.

Serum Tg, measured before surgery during L-T₄ treatment in 24 patients, was undetectable in 10, ranged from 2–10 ng/mL in 9, and ranged from 11–110 ng/mL in the others. Serum Tg, measured in the 52 patients without serum interference after L-T₄ withdrawal, was undetectable (<1 ng/mL) in 8 patients, ranged from 1–10 ng/mL in 13 patients, and ranged from 11–750 in the others. In all patients, including those with undetectable Tg, a treatment dose of ¹³¹I was given because the previous ¹³¹I-TBS, performed with either 74–185 MBq or 3.7 GBq, had shown uptake in lymph node areas.

Surgery

Surgical procedures are summarized in Table 2. The extent of lymph node dissection was determined by the preoperative work-up and was extended in some patients based on intraoperative findings with the probe. The intraoperative probe was considered decisive in 20 patients, revealing neoplastic foci either inside sclerosis due to previous surgery (n = 9), at unusual sites behind vessels or in the mediastinum (n = 10), or both (n = 1). It facilitated intraoperative detection of ¹³¹I foci of uptake previously depicted by the preoperative ¹³¹I-TBS in 26 patients. The usefulness of the protocol was confirmed by the postoperative ¹³¹I-TBS, which indicated the completeness of excision in these 46 patients, as ¹³¹I uptake had disappeared. Furthermore, in 22 of these 46 patients, the probe permitted the discovery and thus the excision of 38 metastatic lymph nodes (1–6/patient) not shown by the ¹³¹I-TBS. They represented 15% of all neoplastic foci. These lymph nodes were located in the central compartment of the neck (13 patients), the jugulo-carotid chain (8 patients), and the internal mammary chain (1 patient).

A total of 257 neoplastic foci were diagnosed at histological examination. Among these, 68 were not shown by the preoperative high dose ¹³¹I-TBS, but 38 of these were demonstrated by the probe. Thus, 30 lymph node metastases among 14 patients (1–8/patient), revealed by neither ¹³¹I-TBS nor the probe, were found only at histological examination of surgical specimens. Among these 30 lymph node metastases, only 6 were micrometastases (Table 5).

Morbidity of surgery was low. One hemomediastinum was observed in a patient in whom a large mediastinal lymph node metastasis was removed through the cervical incision. One patient had a transient laryngeal nerve palsy, but postoperative hypocalcemia did not occur.

For radioprotection studies, measurements were performed during 3 surgical procedures (mean duration, 3 h), 5 days after the administration of 3.7 GBq (100 mCi) ¹³¹I. The mean radiation dose received during each surgical procedure was 40 µSv to the right hand, 70 µSv to the left hand, and 13–15 µSv to the neck.

Postoperative TBS

A postoperative TBS performed with the remaining ¹³¹I activity confirmed the disappearance of uptake in metastasis in 46 patients and the persistence of foci of uptake in 8 patients, who were considered either as pitfalls (n = 4) or as false positive ¹³¹I-TBS results (n = 4).

Follow-up

The 54 patients were followed up for 6 months to 9 yr (mean, 2.3 yr) after surgery. The annual clinical neck examination was normal in all patients.

Serum Tg levels measured during L-T₄ treatment in 47 patients 3 months or more after surgery were undetectable in 41 and ranged from 2–10 ng/mL in the other 6 patients.

Thirty-four patients had ¹³¹I-TBS within 1 yr after surgery with a dose of either 74–185 MBq (n = 22) or 3.7 GBq (n = 12). ¹³¹I-TBS showed an absence of uptake in the 31 patients in whom surgery was assessed as complete and persistent uptake in the neck in 3 patients who were considered pitfalls. The Tg level was measured in 33 patients while off L-T₄ therapy; it was undetectable in 25 patients, ranged from 1–10 ng/mL in 4 patients, and ranged from 11 to 55 in 4 patients.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The present study shows the usefulness of combining high dose ¹³¹I and surgery for patients with positive ¹³¹I uptake in lymph node metastases from differentiated thyroid carcinoma.

Patients were selected on the basis of ¹³¹I uptake in the neck outside the thyroid bed seen on a previous ¹³¹I-TBS. Relatively low (<10 ng/mL) or even undetectable Tg levels while off L-T₄ treatment were observed in 21 patients and may have been related to previous ¹³¹I treatments. However, lymph node metastases were found in 19 of these patients at surgery. This indicates that the Tg level alone, even when measured while off L-T₄ treatment, cannot rule out persistent lymph node metastases in patients who have already been treated with ¹³¹I, but nonetheless suggests that disease is limited.

In accordance with previous data (15, 16, 17, 18, 19), the high dose ¹³¹I-TBS appears to be a sensitive tool for localizing neoplastic foci with ¹³¹I uptake; it permits accurate localization of previously visualized neoplastic foci and the discovery of foci not shown by a ¹³¹I-TBS performed with 74–185 MBq in more than 50% of patients. The other imaging techniques did not show any other lesions, except in 2 patients in whom CT scan showed larger mediastinal lymph node metastases than initially expected with the ¹³¹I-TBS. Surgical excision of neoplastic foci may be difficult in these patients and is facilitated by accurate localization on the preoperative ¹³¹I-TBS and the use of an intraoperative probe. Intraoperative uptake of ¹³¹I in thyroid lymph node metastases was clear-cut in all patients with this protocol. The probe made a major contribution to the operative procedure in 86% of patients (in 22% for unusual sites, in 20% for neoplastic foci embedded in sclerosis, and in 44% for easy localization of neoplastic foci). Furthermore, in 42% of patients, it rendered detectable uptake in lymph node metastases that was too low to be visualized by ¹³¹I-TBS, but was accessible to probe sensitivity. Finally, it confirmed the completeness of surgical excision.

Preoperative administration of high dose ¹³¹I also allows verification of the completeness of surgical excision, as residual activity can be used for a TBS a few days after surgery. The results of this TBS were in close agreement with follow-up data, including Tg measurement while off L-T₄ treatment and ¹³¹I-TBS.

Morbidity was low with this protocol. No infections were observed, and the radiation dose received by the surgeon, and in particular by his fingers, was low and clearly acceptable. The radiation dose received in one surgical procedure is equivalent to 3 days of exposure to natural radiation in Western Europe. The left hand sustained a significantly higher dose than the right hand, probably due to the fact that the surgeon was right-handed and had held the pathological specimens in his left hand.

The results of this study indicate that complete dissection of involved lymph node areas should be highly recommended, as lymph node metastases undetected by ¹³¹I-TBS or by the probe were found in 26% of patients at histological examination of the surgical specimens. This demonstrates that ¹³¹I uptake may vary from one tumor deposit to another, and this is a further indication for surgery. Also, when surgery is performed, a complete dissection of the affected lymph node area should be preferred to lymph node sampling. Even if en block dissection is the preferred treatment in patients with lymph node metastases, the routine use of this protocol and especially of the probe is recommended. It is likely that excision of neoplastic foci in 20 patients in whom the probe was considered decisive would not have been performed without it.

The long term interest of this protocol remains to be assessed because results have not been compared with the standard care of surgery followed by radioiodine. However, a high remission rate (85% for the whole series of patients and 93% after exclusion of false positive ¹³¹I-TBS) was obtained after surgery, which was confirmed during follow-up by negative ¹³¹I-TBS in all patients and by undetectable Tg levels in 73%. These results appear to be significantly better than those reported in previous series in which the rate of apparent complete remission after surgery alone for persistent or recurrent disease is only 40% (13, 22). Similarly, after radioiodine treatment alone, the apparent cure rate is low in patients with easily palpable lymph node metastases or with a relatively low radioiodine uptake (14). Therefore, we are currently using this protocol in our Institution.

No particular risks are associated with this protocol, but optimal collaboration is needed between the departments of nuclear medicine and surgery.

	Acknowledgments

 
We are indebted to Lorna Saint-Ange for editing the manuscript.

Received February 25, 1998.

Revised April 13, 1998.

Accepted May 1, 1998.

	References

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