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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 3 989-994
Copyright © 2000 by The Endocrine Society

Original Studies

Embolization for Vertebral Metastases of Follicular Thyroid Carcinoma

Jan W. A. Smit, G. Jan Vielvoye and Bernard M. Goslings

Departments of Endocrinology (J.W.A.S., B.M.G.) and Radiology (G.J.V.), Leiden University Medical Center, NL 2300 RC Leiden, The Netherlands

Address correspondence and requests for reprints to: Jan W. A. Smit, Department of Endocrinology, Leiden University Medical Center, P.O. Box 9600, NL 2300 RC Leiden, The Netherlands. E-mail: jsmit{at}mail


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Case Reports
 Discussion
 References
 
The technique of selective embolization has been applied for years in the treatment of vascular anomalies, severe hemorrhage and benign or malignant tumors, notably vertebral metastases of renal cell carcinoma. Because this technique is relatively easy to perform and offers immediate relief of symptoms, it is an attractive option for patients with vertebral metastases of thyroid carcinoma with signs of spinal cord compression. In these patients, other treatment modalities like radioactive iodine, external irradiation, or surgery are more cumbersome or less effective in the short term. We describe four patients with metastasized follicular thyroid carcinoma, presenting with neurological symptoms due to vertebral metastases. All patients had undergone total thyroidectomy, ranging from 1 month to 4 yr before embolization. Embolization was combined with iodine-131 therapy when appropriate. Selective catheterization of the arteries feeding the metastases was performed, followed by infusion of polyvinyl alcohol particles (Ivalon). The procedure was technically successful in all patients without adverse effects. In the patients described, embolization resulted in rapid resolution of neurological symptoms, sometimes within hours. The therapeutic effect lasted from months to years. We conclude that embolization of vertebral metastases of follicular thyroid carcinoma is an attractive palliative therapeutic option that may offer rapid relief of symptoms.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Case Reports
 Discussion
 References
 
ARTIFICIAL embolization as a therapeutic modality was introduced more than 30 years ago in the management of arterio-venous malformations (1). In the following decades, the technique of selective embolization has been extended from the treatment of vascular lesions, like arterio-venous malformations (1, 2, 3), hemangiomas (4, 5) and aneurysmal bone cysts (6) to severe hemorrhage (7, 8) and preoperative and therapeutic management of well vascularized benign and malignant tumors. Most reports concerning the latter indication include the embolization of tumors of the head and neck region (9, 10), and osseous metastases from various tumors (11, 12, 13, 14), notably skeletal metastases from renal cell carcinoma (15, 16, 17). Abdominal tumors or metastases have also been embolized (18, 19), sometimes combined with chemotherapy (20). Various natural and synthetic materials such as dura/isobutyl, gelfoam, and polyvinyl alcohol have been used to this end (8, 21, 22).

Ripp et al. (23) described a case of metastatic thyroid carcinoma of the mandible mimicking an arterio-venous malformation. The patient was operated on after ligation of the external carotid artery feeding the tumor. In their comment they stated that "The recent use of embolization to occlude the artery feeding the tumor, should be kept in mind by those faced with similar problems." Camille et al. (22) were the first to report on the preoperative use of embolization in four cases of spinal or pelvic metastases from thyroid carcinoma. Since then, few communications on this treatment modality in thyroid carcinoma have been published (24, 25) and its use is briefly mentioned in a few other publications (10, 13). In our hospital, experience with embolization techniques in the treatment of vertebral (4, 5) and other tumors is long standing. Because embolization can give rapid relief of pain and neurological symptoms in patients with vertebral metastases from renal cell carcinoma (15, 26), we decided to use this treatment in combination with iodine-131 (131I) to patients with vertebral metastases from follicular thyroid carcinoma (FTC). Here, we describe the case histories of four of these patients.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Case Reports
 Discussion
 References
 
Since 1994, four patients with spinal cord or nerve root compression caused by vertebral metastases from FTC have been treated with selective embolization. The data with regard to clinical features, tumor stage, and prognostic score according to the TNM system (27) and details of the embolization procedures of each patient are presented in Tables 1Go and 2Go. All patients had undergone total thyroidectomy previously. Patients 1 and 3 had received 131I therapy earlier in the course of their disease. In patients 2 and 4, the first presentation of thyroid carcinoma was neurological symptoms caused by vertebral metastases. They were referred for 131I therapy after thyroid surgery. Informed consent was obtained from all patients.


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  		Table 1. Characteristics of four patients with vertebral metastases of FTC undergoing embolization

 

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  		Table 2. Characteristics of embolization in four patients with vertebral metastases of FTC

 
All 131I therapeutic doses in our hospital were given after a low-iodine diet preparation of 4 days (28). The first embolization in patient 1 was performed as an emergency procedure to prevent worsening of cord compression and in preparation of an operation on the following day. 131I could only be given 2 months later. Subsequently, we hypothesized that the reversed order, giving 131I therapy first and performing embolization 3–6 days later, might be more beneficial, allowing 50–75% of the radiation dose to be delivered first during one to two effective half-lives of the isotope before interrupting the vascular supply of the tumor. All later embolization procedures were, therefore, carried out in that order.

In general, embolization was performed as: after localizing the metastatic lesion by magnetic resonance imaging (MRI) or computed tomography (CT), the arteries feeding the involved vertebra, branching from the thyreocervical, intercostal, or lumbar arteries, respectively, are visualized by selective catheterization. When a pathological vascular pattern was recognized and it had been verified that no vital structures are supplied by the particular vessel, particles of polyvinyl alcohol (Ivalon; Laboratoires Nycomed S.A., Paris, France) are injected. Generally, Ivalon particles ranging from 300–600 micron were used in quantities depending on the extent of the tumor vasculature (usually up to 100 mg) and suspended in a solution of contrast medium and normal saline. Success of embolization was verified by angiography after the procedure. Possible side effects of the embolization technique are reviewed in "Discussion."


   Case Reports
Top
 Abstract
 Introduction
 Patients and Methods
 Case Reports
Discussion
 References
 
Patient 1

A 49-yr-old male underwent a total thyroidectomy for a FTC in the right thyroid lobe, followed by radioiodine ablative therapy with 2800 MBq 131I. Total-body scintigraphy (TBS) after ablation revealed no distant metastases. The TNM classification after thyroidectomy (pTNM) was T3-N0-M0, stage II. During the course of his disease, vertebral metastases developed, giving rise to episodes of spinal cord compression. Clinical data are presented in Tables 1Go and 2Go.

Four years after thyroidectomy, the patient experienced symptoms of back pain irradiating along the left side of his chest and unsteadiness in his gait. The symptoms worsened within 3 weeks. At admission his gait was ataxic, with paraparesis of both legs and incontinence for urine. Serum Tg was 21 ug/L. MRI disclosed a metastasis in Th6 with spinal cord compression. Embolization of the 6th intercostal artery was carried out (Fig. 1Go). The next day, muscle strength in both legs had improved and the ataxia disappeared. Subsequently, tumor resection was attempted but appeared not to be radical. One month after embolization, MRI no longer revealed spinal cord compression at Th6, but residual tumor was still present. Therefore, radioiodine therapy (6100 MBq) was given 3 months after embolization, but no uptake in Th6 was observed. Therefore, external irradiation (40 Gy) was given, as well. Neurological recovery was complete 9 months after embolization. Tg at that time was 12 ug/L.



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  		Figure 1. Case 1. Embolization of the left intercostal artery Th6. Situation before and after embolization.

 
Six years after thyroidectomy, 4 yr after the first embolization, the patient developed progressive back pain without other neurological defects. MRI disclosed recurrent tumor at Th6 with cord compression. CT of the thorax revealed pulmonary metastases. Tg was 58 ug/L. Embolization of Th6 was carried out. This time, the tumor was supplied by the right 5th and both 6th intercostal arteries. The symptoms subsided within 1 week after embolization.

Six years and 7 months after thyroidectomy, 7 months after the previous embolization, the back pain returned along with ataxia. MRI revealed recurrent spinal cord compression at Th6, and Tg had risen to 111 ug/L. Embolization was repeated, leading to relief of pain within 1 week and disappearance of ataxia. Tg 6 months after the third embolization had remained stable (101 ug/L), despite progressive pulmonary metastases. MRI performed 7 months after this embolization no longer revealed cord compression at Th6. The patient remained free of symptoms for more than 1 yr after this embolization. In this period, he was able to make a solo Atlantic crossing. At this moment, he is still alive but suffer-ing from progressive vertebral and pulmonary metastases.

Patient 2

A 60-yr-old male is reported with a FTC, pT2-N0-M1, stage IV, who presented with severe spinal cord compression (Tables 1Go and 2Go). Symptoms started with thoraco-lumbal back pain for which he consulted a chiropractor. Five months later, he was admitted to another hospital with severe back pain and acutely developed paraparesis of both legs. On CT scan, metastatic lesions were noted in Th7, L2, the right clavicle, and the left sacroiliac region. A needle biopsy of L2 disclosed FTC. He was given 21 Gy external irradiation onto Th7. Nevertheless, 11 days after admission, neurological symptoms progressed to complete paralysis. Laminectomy of Th7 was attempted at that day but was unsuccessful because of severe hemorrhage. Eight days later, a total thyroidectomy was performed. The patient was transferred to our hospital 3 days after thyroidectomy.

At presentation, there was a flaccid paralysis of both legs, hypesthesia from dermatome Th7 downward and fecal and urinary incontinence. MRI disclosed an additional metastasis in C7 with imminent cord compression and an almost complete compression at the level of Th7 (Fig. 2aGo). Tg was 16,841 ug/L (off T4 therapy). Embolization of the bilateral feeding arteries of C7 arising from the thyreocervical trunk was performed 6 days after thyroidectomy to avert loss of function in the upper extremities (Fig. 3Go). The situation at the level of Th7 was deemed hopeless. Four weeks after thyroidectomy, 5600 MBq 131I was given. On TBS, multiple bone metastases were visualized (Fig. 4aGo). In accordance with the patient’s wish to get all possible palliative treatment, it was decided to embolize the lesions in Th7 and L2. Three days after 131I treatment, 1 month after thyroidectomy, bilateral embolization was carried out of the intercostal arteries Th6, Th7, and Th8 and of the feeding arteries of the tumor in L2. The effect of treatment was dramatic: the day after embolization, he felt micturition urge. Five days after embolization, strength of various muscle groups of the legs began to return. Three weeks after embolization, strength had further improved and the patient could be mobilized. Four months later, he was able to walk behind a wheelchair and independently of any aid shortly thereafter. After a period of paresthesias, his sense of feeling in the lower body had returned to normal. A CT scan, 1 month after embolization, no longer showed spinal cord compression at C7, Th7, and L2, with further tumor regression at MRI 5 and 14 months after embolization (Fig. 2bGo).



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  		Figure 2. Case 2. T-1 weighted MRI of the vertebral column. Metastases of follicular thyroid carcinoma causing spinal cord compression at C7 and Th7. Situation before embolization (a) of C7 and Th7 and 15 months after embolization (b).

 


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  		Figure 3. Case 2. Catheterization and embolization of the thyreocervical trunk, feeding the metastasis at C7. a, Before embolization. b, After embolization.

 


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  		Figure 4. Case 2. Whole body scintigraphy after a therapeutic dose of 131I. a, Situation directly after the embolization at C7 and Th7. b, situation 5 months later.

 
Five months after the first dose, he was given a second dose of 6100 MBq 131I. Tg (after withdrawal of T4) was 11,182 ug/L. TBS showed persistent, but diminished, uptake in many metastases and one new localization (Fig. 4bGo). Specifically, there was almost no decrease in uptake at C7, which was embolized before the first 131I treatment, in contrast with the clearly decreased uptake at Th7 and L2, which were embolized after 131I therapy. Angiography of C7 was repeated but showed no abnormal vascularization. Serum Tg decreased to 15 ug/L 12 months after thyroidectomy and started to rise slowly thereafter.

He remained free of symptoms until 6 yr after thyroidectomy, when he developed symptoms of a metastatic lesion in the left acetabulum, for which he was treated with 40 Gy external irradiation at the time of this report.

Patient 3

A 69-yr-old female is presented with an FTC, pT(unknown)-N0-M1, stage IV, with spinal cord compression due to metastasis at L1 (Tables 1Go and 2Go). The patient had undergone a subtotal hemithyroidectomy for what was considered to be a follicular adenoma 14 yr before presentation at another hospital with low back pain. A CT scan disclosed a lytic lesion in L1, which after needle biopsy proved to be a metastasis from a FTC. A total thyroidectomy was performed, but no tumor was found in the removed tissue. Unfortunately, no tissue samples from the previous hemithyroidectomy were available for reevaluation. Subsequently, she was treated with 20 Gy external irradiation and four doses of 1850 MBq 131I at 3-month intervals. TBS showed no other tumor localizations. The back pain decreased during these treatments, but never subsided completely.

She was referred to our hospital 2 yr and 3 months after completion thyroidectomy because there was radicular pain from segment L1 at the left side accompanied by hypesthesia. MRI disclosed a metastatic lesion in L1 with cord compression. Serum Tg on T4 treatment was 267 ug/L 3 months earlier and rose to 1522 ug/L after withdrawal of T4. A therapeutic dose of 6100 MBq 131I was given. TBS revealed uptake in L1. Three days later, embolization of the left intercostal arteries Th12 and L1 was performed. She experienced clear improvement within 2 days after the embolization and could resume normal physical activity without pain in 4 weeks. Tg decreased moderately to 163 ug/L 12 months after treatment. Although she was without complaints at that time, it was decided to give her a second combined treatment course with 131I therapy and embolization, 3 yr and 6 months after thyroidectomy, 1 year and 3 months after the first embolization. TBS revealed persistent uptake in L1. Tg further decreased to 95 ug/L after this procedure. For personal reasons, she was referred back to her regional hospital, where 3 years later she is still ambulant.

Patient 4

A 69-yr-old male is described with FTC pT4-N1-M1, stage IV, who developed spinal cord compression due to vertebral metastases at L3 and L4 (Tables 1Go and 2Go). He underwent a total thyroidectomy with modified radical neck dissection on the right side for an insular type FTC with extrathyroidal tumor growth and several lymph node metastases on the right side of his neck.

Seven weeks after thyroidectomy, he was referred to our hospital because of low back pain irradiating to the left leg, which seemed to have been present for 2 months. A CT scan disclosed a lytic lesion in the body of L4 with cord compression and pulmonary metastases. Tg after thyroid hormone withdrawal was 574 ug/L. An ablation dose of 131I was given. TBS revealed activity in the neck, lungs, and at L4. Six days thereafter, 2 months after thyroidectomy, the arterial branches from the left and right lumbar arteries feeding the tumor in L4 were injected with Ivalon. Immediately after the embolization, the back pain resolved and he could resume normal physical activity within 2 months after embolization. In view of the generally aggressive behavior of insular type FTC, 40 Gy external irradiation was given 2 months after embolization. A CT scan, performed 3 months after embolization, no longer revealed cord compression. Tg was 25 ug/L at this time. Subsequently, a therapeutic 131I dose of 6300 MBq was given. TBS showed uptake in the known tumor localizations, including L4. Twelve months after embolization, 131I therapy was repeated. Tg after withdrawal was 688 ug/L. This time, activity at L4 was diminished and angiography revealed no pathological vascularization of L4.

Two years after thyroidectomy pain returned. Tg on T4 therapy was 380 ug/L, and MRI revealed a new metastasis at L3, giving rise to spinal cord compression. Embolization of the arteries branching from the lumbar arteries was performed. Symptoms resolved immediately, but Tg levels rose steadily. A surgical stabilization procedure was performed 2 months after this embolization, to prevent collapse of the affected vertebra. However, 1 month after this procedure (2 yr and 3 months after thyroidectomy), pain returned, this time accompanied by paresis of both legs caused by progressive cord compression at L3. Tg was 607 ug/L. Embolization of L3 was repeated. Strength of his legs improved within 2 weeks, although his neurological condition did not return to normal. Tg 5 months after the third embolization had only slightly risen to 630 ug/L. MRI 7 months after this embolization revealed diminished cord compression at L3. At the time of this report, he is able to move about at home with the help of a walking aid.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Case Reports
 Discussion
References
 
In the present study, we describe the technique of selective embolization for vertebral metastases of FTC. Therapeutic options in metastasized thyroid carcinoma are limited, especially when the uptake of radioiodine is insufficient. Nevertheless, as the rate of progression of metastases from thyroid carcinoma is generally moderate, life expectancy for these patients may extend for years. Consequently, quality of life is the most important goal in the management of metastasized thyroid carcinoma. Vertebral metastases, in particular, may impair quality of life to a great extent. Therefore, palliative treatment aimed at preventing or reducing neurological symptoms of vertebral thyroid carcinoma metastases is of great importance. Requirements for palliative treatment include a minimal burden or risk for the patient and a reasonable effectiveness.

In the cases described, the most significant proof of the effectiveness of embolization seemed to be an often immediate relief of neurological symptoms. In patient 1, this effect was observed before additional therapy (external radiotherapy) was given. Because no radioiodine uptake was observed in the metastatic lesion of this patient, the relief of symptoms has to be attributed to the embolization, which is clearly the case for the second and third embolization in this patient, as these were not accompanied by other interventions. The third embolization even caused a temporary fall in Tg levels and tumor regression at MRI. In patient 2, external irradiation had not influenced his severe neurological condition. After embolization, a rapid improvement of his condition was observed, which cannot be explained by the radioiodine therapy that was given shortly before embolization because the effects of radioiodine therapy are generally observed after a longer time interval. However, the final clinical outcome of the first treatment episode has to be attributed to the combined treatment of radioiodine therapy and embolization. The same applies to patient 3 and the first embolization in patient 4, where, in our opinion, the immediate relief of symptoms was the result of the embolization, whereas the longer term clinical outcome may be due to the combined treatment. The second and third embolizations in patient 4 did ameliorate the neurological symptoms, without other interventions. We believe that selective embolization is a valuable addition to the therapeutic strategies for symptomatic vertebral metastases from thyroid carcinoma, because it is less invasive than surgery and offers a faster relief of symptoms than radioactive iodine. However, combined therapy with radioiodine should always be considered, as the long-term effectiveness of radioiodine therapy in skeletal metastases has been demonstrated convincingly (29, 30). When surgery is considered, preoperative embolization may be expected to reduce blood loss during operation, as has been demonstrated in other tumors (17) and suggested for thyroid carcinoma metastases (22). In the cases described above, the intervention was technically successful in all patients. However, sometimes it is impossible to locate or reach the feeding artery of the tumor. In addition, an artery that feeds the tumor may supply vital structures like the spinal cord. In this case, no embolization can be performed. No adverse events occurred in the cases described above. In the literature, adverse events are seldom reported. Erroneous embolization of spinal arteries may result in aggravation of neurological symptoms (12). Hypersensitivity to embolization compounds has been described (19), although this may be hard to distinguish from the so-called postembolization syndrome, characterized by fever caused by tumor necrosis (12). In addition, catheterization in its own may be associated with complications like arteriovenous fistula or aneurysm at the puncture site or cholesterol emboli. A drawback of embolization may be that it induces hypoxia within the tumor, which is a potent thrive for neovascularization (31), thus leading to relapse of tumor. In theory, addition of antiangiogenetic compounds may enhance the effect of embolization.

In conclusion, we believe arterial embolization of vertebral metastases of FTC may offer rapid relief of symptoms even in the presence of severe paraplegia, which may last for a long period of time. As a consequence, this procedure merits to be considered as an attractive therapeutic alternative in the difficult management of patients with advanced metastatic disease.

Received April 30, 1999.

Revised November 2, 1999.

Accepted November 12, 1999.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Case Reports
 Discussion
 References
 

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Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals