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1
Department of Radiology, Mayo Clinic and Mayo Foundation, 200 First St., SW,
Rochester, MN 55905.
2
Division of Endocrinology and Internal Medicine, Mayo Clinic and Mayo
Foundation, Rochester, MN 55905.
3
Department of Surgical Pathology, Mayo Clinic and Mayo Foundation, Rochester,
MN 55905.
Received July 9, 2001;
accepted after revision September 20, 2001.
Presented in part at the 11th International Congress of Endocrinology,
Sydney, Australia, November 2000.
Abstract
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SUBJECTS AND METHODS. Fourteen patients who had undergone thyroidectomy for papillary thyroid carcinoma presented with limited nodal metastases (one to five involved nodes) in the neck between May 1993 and April 2000. All patients had received previous iodine-131 ablative therapy with a mean total dose per patient of 7,548 MBq. Ten of the patients either were considered poor surgical candidates or preferred not to have surgery, and all were unresponsive to iodine-131 therapy. Each metastatic lymph node was treated with percutaneous ethanol injection, and patients received both clinical and sonographic follow-up.
RESULTS. Twenty-nine metastatic lymph nodes in our 14 patients were injected. Mean sonographic follow-up was 18 months (range, from 2 months to 6 years 5 months). All treated lymph nodes decreased in volume from a mean of 492 mm3 before percutaneous ethanol injection to a mean volume of 76 mm3 at 1 year and 20 mm3 at 2 years after treatment. Six nodes were re-treated 2-12 months after initial percutaneous ethanol injection because of persistent flow on color Doppler sonography (n = 4), stable size (n = 1), or increased size (n = 1). Two patients developed four new metastatic nodes during the follow-up period that were amenable to percutaneous ethanol injection. Two patients developed innumerable metastatic nodes that precluded retreatment with percutaneous ethanol injection. No major complications occurred. All patients experienced long-term local control of metastatic lymph nodes treated by percutaneous ethanol injection. In 12 of 14 patients, percutaneous ethanol injection was successful in controlling all known metastatic adenopathy.
CONCLUSION. Sonographically guided percutaneous ethanol injection is a valuable treatment option for patients with limited cervical nodal metastases from papillary thyroid cancer who are not amenable to further surgical or radioiodine therapy.
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The sonography scanners used in this study were the XP 128 and Sequoia 512 (Acuson, Mountain View, CA). We used the highest frequency transducer that permitted adequate depth penetration—typically 8-15 MHz. Each lymph node was carefully measured, and, whenever possible, color Doppler sonography was performed to document baseline size and nodal perfusion. The mean diameter of the treated lymph nodes was 8.7 mm (range, 4.4-17.2 mm).
The percutaneous ethanol injection technique was based on the procedure that has been used at our institution since 1988 to treat selected parathyroid adenomas [7]. A conventional 3-cm, 25-gauge needle was attached to a tuberculin syringe containing up to 1 mL of 95% ethanol. The skin and soft tissues between the skin and lymph node were anesthetized with 1% lidocaine. We discovered during the study that patients experienced less pain if the tissue surrounding and deep to the lymph node had been anesthetized. In addition, several patients required 1-3 mL of midazolam hydrochloride for sedation. The needle was placed into the lymph node under sonographic guidance using the free-hand technique, which allowed the fine positioning required for complete treatment of each involved lymph node.
Each of the nodes was punctured and injected in multiple sites. Typically, the deepest portion or one of the poles of a node was treated first with a small amount of ethanol (0.05-0.1 mL). As the ethanol was injected, that portion of the node became intensely echogenic from the formation of microbubbles of gas. After a short time, typically less than 1 min, the echogenic zone would decrease, allowing better visualization of the needle. The needle was then repositioned, and the injections were repeated (between three and 10 times) until it appeared that the entire lymph node had been adequately treated (Fig. 1A,1B,1C,1D). The volume of ethanol used in each treated node ranged from 0.1 to 0.8 mL, with a mean of 0.34 mL. Care was taken to inject small amounts of ethanol in each site to prevent diffusion of ethanol along the needle track into surrounding cervical soft tissues. Despite this care, most patients had mild to moderate pain that resolved within minutes.
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The mean number of treatment sessions per patient was two (range, from one to four). Treatment of patients with one or two small easily treated nodes was completed in one session. Patients with larger nodes that were deeply situated or difficult to treat required multiple sessions, as did patients with nodes that showed evidence of residual perfusion on color Doppler sonography. As we gained experience, we came to favor a minimum of two treatment sessions. All percutaneous ethanol injection treatments were done by one of three radiologists. Typically, treated patients received routine clinical and sonographic follow-up every 3 to 6 months. The follow-up period ranged from 2 months to 6 years 5 months (mean, 18 months).
The pretreatment volume of each lymph node was calculated using the anteroposterior, transverse, and longitudinal measurements. Similarly, volumes were calculated using sonograms from each subsequent follow-up. All sonographic examinations included a diagram of the location of each node to ensure accurate communication (Fig. 2A,2B), and the relative increase or decrease of nodal volume was calculated for each node at each follow-up examination. In addition, we evaluated the presence or absence of blood flow in each previously treated lymph node using color-flow Doppler sonography. Treatment was considered to have failed in those patients whose injected nodes either enlarged or showed evidence of persistent perfusion on color Doppler sonography or power Doppler sonography after percutaneous ethanol injection. We regarded treatment as successful in patients in whom the size of the lymph nodes on follow-up images had decreased and in whom there was no residual evidence of perfusion.
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The mean volume of the treated metastatic lymph nodes was 492 mm3 prior to percutaneous ethanol injection and decreased to a mean volume of 76 mm3 after 1 year and 20 mm3 after 2 years (Figs. 3A,3B,3C and 4). Nine lymph nodes in seven patients disappeared during the follow-up period.
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Five patients had initial treatment failures that were confirmed on follow-up sonography 2-12 months after treatment. Three of these patients had one lymph node with at least some residual flow detected on color Doppler sonography (Fig. 5A,5B,5C,5D). In one patient, the size of one lymph node initially increased, and flow persisted in another node. One patient had a lymph node that was unchanged on the follow-up sonogram. All five of these patients were successfully re-treated; on follow-up sonographic examinations, the size of the nodes had decreased and no perfusion was evident. In this group of patients, there were no long-term treatment failures. Two patients developed multiple metastatic cervical lymph nodes during the follow-up period that were too numerous to treat. In these two patients, percutaneous ethanol injection was successful in treating nodal metastasis, but there was progression elsewhere in the neck.
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Most patients experienced brief discomfort at the injection site, likely related to local extravasation of a small amount of ethanol into the surrounding cervical soft tissues. Several patients reported pain extending into the jaw or chest. In all of these patients, the discomfort resolved after several minutes. Patients who received local anesthesia deep to the treated lymph node, as well as in the superficial tissues, had less pain. No patient experienced transient or permanent hoarseness or vocal cord paralysis. No serious complications occurred in the group.
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Several treatment options are available for patients with papillary thyroid carcinoma and metastatic lymphadenopathy. Radioiodine therapy is a common treatment option, but it has varying rates of success in treating metastatic adenopathy [11]. Given the indolent nature of the disease, "watchful waiting" is an option for some patients, including the elderly, those who are poor surgical candidates, or those who are considered at low risk. Many younger patients in whom radioiodine therapy has failed or who had disease that was already at stage III at initial surgery usually receive further neck exploration and metastatic lymph node resection [12]. Surgery may be overly aggressive treatment in some patients. It is more difficult in the patients who have had a previous neck dissection or external beam radiation, and there may be a limit as to how many reexplorations can be safely attempted.
Our study has shown that percutaneous ethanol injection is a viable treatment option for patients with limited cervical lymph node metastases. All cases of treated metastatic adenopathy responded with a dramatic reduction in nodal volume and a lack of nodal perfusion. Approximately one third of treated nodes disappeared completely. To achieve this favorable result, five of the 14 patients required retreatment 2-12 months after their initial treatment. This finding suggests that metastatic nodes should be treated in at least two sessions on subsequent days to ensure adequate treatment.
Color Doppler sonography was extremely helpful in revealing regions of persistent nodal perfusion and permitting accurate targeting of these regions. Treatment of metastatic nodes should be repeated until nodal perfusion is no longer present on color Doppler sonography. The technique requires a degree of technical expertise that is similar to that required for sonographically guided lymph node biopsy [13] or percutaneous ethanol injection of a parathyroid adenoma [7]. In centers with personnel who have such experience, the technique is readily transferable.
There were no complications in this series, although a potential risk of this technique is nerve damage caused by ethanol extravasation. The risk can be reduced by injecting only extremely small volumes of ethanol, typically 0.1 mL or less, into each site. Ethanol extravasation outside the node can be visualized, and injection in that location should be terminated whenever extravasation occurs or the patient experiences considerable pain. The risk of ethanol extravasation can also be reduced by identifying the position of the needle tip within the node before proceeding with the injection.
Advantages of percutaneous ethanol injection of metastatic lymph nodes over conventional therapy options are many. Percutaneous ethanol injection is far less invasive than surgical neck exploration and can be repeated many times without increased technical difficulty. Its cost is much less—a total procedural cost of $836 versus surgical neck exploration cost of $9,800-12,000. Iodine-131 therapy costs $1,200-1,480 on average. (All costs given are based on Medicare reimbursement rates.) Percutaneous ethanol injection has little or no morbidity and is done on an outpatient basis; the patient can resume normal activities almost immediately. Patients avoid the morbidity, hospitalization, and general anesthesia required for neck exploration. Percutaneous ethanol injection appears to be more effective than radioiodine therapy without the risks, systemic symptoms of hypothyroidism, or required hospitalization. It gives clinicians an inexpensive, effective, virtually risk-free option for patients who might otherwise be considered for watchful waiting. A repeated exploration and radioiodine therapy are still the most appropriate treatments for patients with widely metastatic adenopathy and perhaps for those with a more aggressive form of papillary thyroid carcinoma. In our study, two patients with an aggressive form of papillary thyroid carcinoma had their initial nodes treated successfully but developed widespread metastatic lymph nodes during the follow-up period.
The need for an effective, less invasive treatment option has led to the evaluation of other sonographically guided percutaneous ablative techniques. Two groups of researchers have described using radiofrequency ablation to treat metastatic nodes from papillary thyroid carcinoma. Solbiati et al. [14] treated two recurrent 1.5- to 2.0-cm nodal metastases in two patients who were no longer considered surgical candidates. Radiofrequency ablation was performed for 12 min using a 17-gauge, internally cooled electrode (Radionics, Billerica, MA). Both lymph nodes were necrotic on the 12-month follow-up sonograms. These two patients had no complications. Dupuy et al. [15] reported on eight patients with metastatic adenopathy from papillary thyroid carcinoma. Treated nodes were larger than in our patient group, measuring 0.8-4.0 cm (mean, 2.4 cm). Radiofrequency ablation was performed for 2-6 min using a 17- gauge, internally cooled electrode. Radiofrequency ablation provided good local control of treated lymph nodes, but in four of eight patients, the disease progressed elsewhere in the body. One patient suffered vocal cord paralysis, and one developed a skin burn.
Percutaneous ethanol injection has several possible advantages over radiofrequency ablation. Treatment with percutaneous ethanol injection requires less than 1 mL of ethanol at a cost of $1.89/10 mL vial, whereas a radiofrequency ablation requires electrodes that cost approximately $500 each. During percutaneous ethanol injection, the extent of ethanol diffusion into the node is seen as an echogenic region in most patients. This visibility helps one to monitor the volume of ethanol injected at each site and to avoid major extravasation of ethanol and damage of adjacent structures. In contrast, the exact extent of radiofrequency ablation cannot be identified on sonography. Radiofrequency ablation has a higher potential of collateral damage to adjacent structures, such as the recurrent laryngeal nerve. Radiofrequency ablation has advantages in scirrhous neoplasms that do not permit adequate diffusion of ethanol. However, papillary thyroid carcinoma is a relatively "soft" neoplasm, and ethanol readily diffuses into the node. Percutaneous ethanol injection can be performed with only local anesthesia in most patients, and the pain is minor and transient. Radiofrequency ablation is more painful and usually requires heavy IV sedation. Radiofrequency ablation has an advantage in that only one treatment session is required rather than the average of two outpatient sessions for our patients treated with percutaneous ethanol injection.
Papillary thyroid carcinoma is an indolent disease with 20-year survival rates exceeding 90%. Some might suggest that our follow-up period may not have been long enough to determine the impact on recurrence rates, given the slow course of this disease. However, close imaging studies performed at follow-up showed no patients with recurrent growth in treated nodes, and nine treated lymph nodes had completely disappeared. Imaging follow-up should be a more sensitive method of tracking early disease progression than survival rates in patients with metastatic nodes.
Our study clearly did not examine the question of whether treating metastatic adenopathy with percutaneous ethanol ablation had any impact on patient survival. It is, however, well recognized that nodal metastases in papillary thyroid carcinoma do not portend a poor prognosis [4, 8] and are not associated with increased mortality. Given the indolent nature of papillary thyroid carcinoma, a large prospective study with a long follow-up period for selected high-risk patients might be necessary to determine if percutaneous ethanol injection of nodal metastases has an impact on survival. However, our study results do clearly show that percutaneous ethanol injection is an effective, safe, and inexpensive treatment option for treating metastatic lymph nodes, making the need to show improved survival less compelling. If elimination of all microscopic residual neck disease is required to cure papillary thyroid carcinoma, such a goal may be achieved through the combination of sonographic surveillance and selective use of percutaneous ethanol injection in patients with recurrent nodal disease that is not amenable to conventional retreatment with surgery, radioiodine, or external irradiation.
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