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(Radiology. 2000;217:673-677.)
© RSNA, 2000

Vascular and Interventional Radiology

Thyroid Tissue: US-guided Percutaneous Interstitial Laser Ablation-A Feasibility Study1

Claudio M. Pacella, MD, Giancarlo Bizzarri, MD, Rinaldo Guglielmi, MD, Vincenzo Anelli, MD, Antonio Bianchini, MD, Anna Crescenzi, MD, Sara Pacella, MD and Enrico Papini, MD

1 From the Departments of Diagnostic Imaging (C.M.P., G.B., V.A., A.B., A.C., S.P.) and Endocrine, Metabolic, and Digestive Diseases (R.G., E.P.), Regina Apostolorum Hospital, Via San Francesco, 50, 00041 Albano Laziale, Rome, Italy. From the 1998 RSNA scientific assembly. Received August 3, 1999; revision requested September 20; final revision received March 2, 2000; accepted March 7. Address correspondence to C.M.P (e-mail: cmpac@tin.it).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate percutaneous interstitial laser photocoagulation (ILP) as a palliative treatment of recurrent thyroid carcinoma untreatable with surgery or radioiodine administration.

MATERIALS AND METHODS: By using 18 resected thyroid glands, the volume and histologic pattern of ILP-induced thyroid damage were assessed. In vivo treatment feasibility was evaluated by using a low-energy laser in two volunteers before thyroidectomy for huge autonomously functioning nodules. With ultrasonographic (US) monitoring, a 21-gauge spinal needle was inserted into the thyroid nodules. A 300-µm quartz fiberoptic guide was inserted through the needle lumen, and the fiber tip was placed in direct contact with the tissue. Laser irradiation was performed with a 1.064-nm Nd:YAG laser in surgically resected glands, which were treated with 2, 3, 5, or 7 W.

RESULTS: Tissue ablation was well-defined histologically, and its area was related to laser irradiation parameters (range, 0–26 mm). No correlation was found between US images and the actual extent of laser-induced lesions. Large colloid or fluid collections did not permit regular heat diffusion within the tissue. In vivo low-energy ILP was performed without technical difficulties or complications.

CONCLUSION: ILP induces well-defined tissue ablation correlated with energy parameters in thyroid glands devoid of cystic areas. ILP could be a therapeutic tool for highly selected problems in thyroid tumor treatment.

Index terms: Interventional procedures, 273.1267, 273.12985 • Lasers, interstitial therapy, 273.1267 • Thyroid, neoplasms, 273.367 • Thyroid, therapeutic radiology, 273.1267, 273.12985 • Thyroid, US, 273.12985


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Ultrasonographically (US) guided ablation of thyroid tissue by means of percutaneous ethanol injection was proposed in 1990 (1). The procedure was applied to the treatment of autonomously functioning thyroid nodules and cystic thyroid nodules, and the results of several studies (2–7) have demonstrated its effectiveness and safety. However, percutaneous ethanol injection does not ablate tissue with a regular, homogeneous, and reproducible pattern in a single application, and it seems not to be suitable for the ablation of neoplastic tissue (6). Light may be delivered interstitially by implanting a laser fiber directly into the tissue (8,9). Interstitial laser photocoagulation (ILP) has been applied experimentally (10–15) and clinically (13,16–22), with varying degrees of success in tumoral tissue ablation in various organs (15).

We evaluated the efficacy of ILP in inducing thyroid tissue ablation. The aim of our study was to obtain a potential therapeutic tool for palliative treatment of recurrent thyroid carcinomas that are untreatable with surgery or radioiodine administration. We sought to determine, by means of repeated observations, (a) the feasibility of US-monitored insertion of a laser-coupled optical fiber into thyroid glands; (b) the laser-power output that, with minimal vaporization and charring, would produce a thermal lesion of potentially useful volume; (c) the volume and histologic pattern of thyroid tissue damage induced by ILP and its correlation with laser parameters in surgically resected thyroid glands; and (d) in vivo treatment safety in two volunteers about to undergo thyroidectomy necessitated by large autonomously functioning thyroid nodules.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Ex Vivo ILP of Surgically Resected Thyroid Glands
The first part of our study was performed in 18 thyroid glands obtained from patients who had undergone total thyroidectomy because of Graves disease or large goiter. Six of the 11 multinodular goiters manifested as large colloid nodules. Malignancies previously were ruled out in all patients by means of US evaluation, multiple fine-needle aspiration biopsies, and macroscopic evaluation of the excised glands. Surgical specimens were laser treated immediately after excision.

A commercially available US scanner (AU 930; Ansaldo Esaote, Genoa, Italy) with a 10-MHz linear transducer was used for all procedures. In each experiment, a 75-mm 21-gauge spinal needle (Becton-Dickinson, Rutherford, NJ) was implanted into thyroid glands with US guidance. The needle tip was positioned at least 15 mm below the surface of surgical specimens and at least 20 mm from a previous laser-induced lesion. The laser light was delivered via a plane-cut fiberoptic waveguide (Medical Energy, Pensacola, Fla) with an outer diameter of 300 µm, including the protective outside coating. The optical fiber was inserted through the sheath of the needle, which was then withdrawn 5 mm, leaving the fiber tip in direct contact with the tissue. Laser energy from a continuous-wave Nd:YAG laser (D.E.K.A., Florence, Italy) operating at 1.064 nm was delivered interstitially into the thyroid tissue through the optical fiber.

Surgical specimens were subdivided into four groups and exposed to different total energy outputs: Laser output power was maintained at 2, 3, 5, or 7 W by using appropriate exposure times, with a total delivered energy of 500, 1,000, 1,500 or 2,000 J, respectively (Tables 1–3). ILP was performed by using the same amount of laser energy at two sites in each surgical specimen lobe to induce two lesions. A total of 52 laser illuminations was performed, four more than were planned, since four could not be evaluated because the presence of large fluid areas blunted the effectiveness of laser ablation. Hence, the number of effective ILP treatments performed in each of the four groups was 12: three treatments for each of the four subgroups of total energy delivery. All laser illuminations were monitored continuously by means of real-time US, and representative static images were recorded (Fig 1).


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  		TABLE 1. Mean and SD of Longitudinal Diameters of Cavitation at Different Levels of Output Power and Delivered Energy
 

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  		TABLE 2. Mean and SD of Transverse Diameters of Cavitation at Different Levels of Output Power and Delivered Energy
 

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  		TABLE 3. Mean and SD of Transverse Diameters of Coagulative Layers at Different Levels of Output Power and Delivered Energy
 


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  		Figure 1a. Longitudinal ex vivo US images obtained before and during laser application with a plane-cut fiber tip at 5.0 W in a resected specimen. (a) Image obtained before ILP clearly shows the tip (arrow) of the plane-cut fiber and the tip (arrowhead) of the needle. (b) Image obtained early in the ILP procedure through the surgically resected thyroid gland shows the tip (solid arrow) of the plane-cut fiber and the tip (arrowhead) of the needle at the beginning of laser irradiation encircled by a roughly spherical hyperechoic area (open arrow) with associated acoustic shadowing. (c) Image obtained late in the ILP procedure at 2,000 J in the same area as in a along the needle. There is a large, hyperechoic, ill-defined area (arrowhead) with associated acoustic shadowing (arrow) around the fiber tip.

 


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  		Figure 1b. Longitudinal ex vivo US images obtained before and during laser application with a plane-cut fiber tip at 5.0 W in a resected specimen. (a) Image obtained before ILP clearly shows the tip (arrow) of the plane-cut fiber and the tip (arrowhead) of the needle. (b) Image obtained early in the ILP procedure through the surgically resected thyroid gland shows the tip (solid arrow) of the plane-cut fiber and the tip (arrowhead) of the needle at the beginning of laser irradiation encircled by a roughly spherical hyperechoic area (open arrow) with associated acoustic shadowing. (c) Image obtained late in the ILP procedure at 2,000 J in the same area as in a along the needle. There is a large, hyperechoic, ill-defined area (arrowhead) with associated acoustic shadowing (arrow) around the fiber tip.

 


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  		Figure 1c. Longitudinal ex vivo US images obtained before and during laser application with a plane-cut fiber tip at 5.0 W in a resected specimen. (a) Image obtained before ILP clearly shows the tip (arrow) of the plane-cut fiber and the tip (arrowhead) of the needle. (b) Image obtained early in the ILP procedure through the surgically resected thyroid gland shows the tip (solid arrow) of the plane-cut fiber and the tip (arrowhead) of the needle at the beginning of laser irradiation encircled by a roughly spherical hyperechoic area (open arrow) with associated acoustic shadowing. (c) Image obtained late in the ILP procedure at 2,000 J in the same area as in a along the needle. There is a large, hyperechoic, ill-defined area (arrowhead) with associated acoustic shadowing (arrow) around the fiber tip.

 
To facilitate comparison with histopathologic findings, the static images were obtained in a nearly sagittal plane angled to include the implanted optical fiber. During laser illumination, US evaluation was used to assess the appearance of the fiberoptic tip, the characteristics and diameters of laser-induced lesions, and the definition of the margins of thermal injury. After laser irradiation, the fiber was withdrawn and the needle removed. The entry point of the fiber and the needle track were marked with a suture, and a diagram of the lesion sites was made for reference at the time of sectioning.

After laser treatment, thyroid glands were cut along the axis of fiberoptic tracts, and adjacent slices were treated in different ways: for each irradiation site, one slice was immediately frozen, and one slice was fixed in formalin and embedded in paraffin. Surgical samples were then submitted for routine examination. Cryostatically removed sections from frozen slices were histochemically stained to determine succinic acid dehydrogenase activity. Paraffin sections from formalin-fixed slices were stained with hematoxylin-eosin for morphologic study of laser-induced lesions. Surgical samples were sectioned, fixed in formalin, embedded in paraffin, and microscopically observed for the diagnostic histologic report (23).

Feasibility of In Vivo ILP Treatment
Between April 1996 and May 1998, the second study was performed in two female volunteer patients 45 and 61 years old. The patients had large (>40 mL) autonomously functioning thyroid nodules that were about to be surgically excised. After they had received adequate information, they gave their written consent to undergo ILP with low-energy output for experimental purposes 1 week before undergoing thyroidectomy.

The study was performed in compliance with the Helsinki Declaration, after the approval of the local bioethics committee, which required that the energy delivered should have been previously demonstrated not to induce lesions exceeding 20 mm in maximum diameter.

After careful cleansing, 1.0–1.5 mL of 2% lidocaine hydrochloride (Xylocaina Astra 2%; Astra, Milan, Italy) was injected slowly into superficial cervical tissue. With US monitoring, a 21-gauge spinal needle was inserted into the thyroid nodules and placed in the center of the lesion. Care was taken to maintain a distance of at least 25 mm between the needle tip and the surrounding cervical structures. After the needle had been fixed in the appropriate position, a 300-µm quartz fiberoptic waveguide was advanced through the sheath of the needle and placed in contact with tissue according to the previously described technique. Each patient underwent a single treatment with laser output power maintained at 5 W by adjusting the exposure time to reach a total energy output of 600 or 1,800 J. The patients were watched for 30 minutes without any medication. No local or general complications were observed.

Seven days after laser illumination, US was repeated to assess the changes over time of the appearance of laser-induced lesions and the measurements of the different constituents—cavitation, charring, and coagulative necrosis—of the complex thermal lesions immediately before surgical excision. Lesion size was measured by means of static images obtained in the transverse, longitudinal, and anteroposterior axes. Images were obtained along the plane of the greatest diameter of the lesion and were measured twice in each patient. Surgical specimens were processed as previously described and measured macroscopically and histologically.

Statistical Analysis
Linear regression analysis was performed to assess the correlation between the energy deposition and the volumes of laser-induced necrosis in ex vivo studies. The mean diameters of the lesions observed at US monitoring during laser irradiation were compared with the dimensions observed at histologic examination by using the Student t test for unpaired data and the analysis of variance, or ANOVA, test. The mean histologic diameters of the lesions obtained with different output powers were compared by using the Student t test for unpaired data and the analysis of variance test. Differences were considered significant when the P value was less than .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
At US monitoring of the resected thyroid glands, the tip of the optical fiber was clearly depicted as a hyperechoic spot. During laser irradiation, an irregular hyperechoic area with associated acoustic shadowing was observed gradually and slowly enlarging over time. The margin of the hyperechoic zone was usually irregular and poorly defined (Fig 1).

At histologic examination, the treated areas were characterized by a central cavity surrounded by a thin layer of carbonized tissue and by an outer stratum of coagulative necrosis. A rim of metabolic damage due to loss of succinic acid dehydrogenase activity encircled the area of coagulative necrosis (Fig 2). Mean measurements of the cavitation along and orthogonal to the fiber axis are summarized in Tables 1 and 2. Mean measurements of coagulative necrosis surrounding the cavitation are summarized in Table 3. The area of tissue ablation was related to laser irradiation parameters (range, 0–26 mm).



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  		Figure 2. Photomicrograph of a frozen section stained for succinic acid dehydrogenase activity shows reduction of enzyme (top left) around coagulative necrosis in one of the volunteers. (Succinic-dehydrogenase stain; original magnification, x400.)

 
US images obtained in vivo during ILP irradiation showed, after a delay of about 80–120 seconds, a hyperechoic area with ill-defined borders around the fiber tip because large colloid or fluid collections did not permit regular heat diffusion within the tissue. This region expanded slowly, and acoustic shadowing made the deep surface of the lesion difficult to identify precisely. The vapor was clearly visible at US as small, hyperechoic foci close to the laser-induced lesion. After 300–400 seconds, a plateau effect was seen, with only slight further expansion of the hyperechoic zone (Fig 3). Hyperechoic streaks radiating from the treated area and directed to the gland surface were visible owing to fluid vaporization and the formation of microbubbles of gas along tissue planes. Sonograms obtained 7 days after ILP showed a complex lesion (Fig 4) characterized by a small central hypoechoic area (zone of vaporization), surrounded by a hyperechoic rim (zone of carbonization) and an outer hypoechoic zone (zone of coagulative necrosis).



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  		Figure 3. Transverse in vivo US image obtained at the end of laser application shows a large, ill-defined hyperechoic area (arrows), with associated acoustic shadowing. The hyperechoic area probably represents microbubbles in heated thyroid tissue.

 


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  		Figure 4. Transverse in vivo US image obtained after laser application. From the center of the lesion outward, a small central hypoechoic cavity (zone of vaporization), surrounded by a hyperechoic rim (arrow) representing debris in the margin of the cavity (zone of carbonization), and a broad hypoechoic area (zone of coagulative necrosis; arrowhead) surrounded by normal thyroid are visible.

 
At macroscopic examination, all the treated areas showed a spindle-shaped, central empty core of vaporization with debris from carbonization in the margin of the cavity. The outer edge of the carbonized area was surrounded by a pale and well-demarcated zone of necrosis. The needle track, connecting the thyroid surface to one pole of the laser-treated elliptic area, showed laser-induced damage in only its distal 3 mm. Surgical specimens obtained in the two patients after ILP showed the same pattern of histologic damage demonstrated in resected glands (Fig 5). The diameters of the lesions were 6.3 x 4.3 mm in the patient treated with 600 J and 16.4 x 12.4 mm in the patient treated with 1,800 J. No correlation (r = 0.11; P = .085) was found between US images and the actual extent of laser-induced lesions.



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  		Figure 5. Photomicrograph of a histologic section from the treated area in one of the volunteers. Coagulative necrosis is observed in the upper left, and hemorrhage is seen to the right of the nodule. (High-power field-strength; hematoxylin-eosin stain; original magnification, x100.)

 
Feasibility treatments were performed without local complications; neither analgesics nor antibiotics were needed after the procedure. During laser irradiation, patients experienced a mild burning pain, which was well tolerated and ceased as soon as the energy was turned off.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
ILP-delivered photons are absorbed within the tissue and induce an increase in temperature, followed by partial denaturation of the irradiated tissue. By using low-energy output (2–5 W per fiber) close to the implanted fiber tip, the temperature exceeds 100°C and results in vaporization of the core of the lesion (8,9). Sufficient laser energy is delivered to heat cells throughout the target volume to temperatures exceeding the protein denaturation threshold (60°C) and causing coagulative necrosis. ILP induced well-defined areas of complete tissue ablation both in surgical specimens and in patients with autonomously functioning thyroid nodules. All tissue included within the radius of interstitial laser ablation appeared vaporized or carbonized or had undergone coagulative necrosis, and no viable cells were observed inside the treated area (14).

The absence of the irregular pattern of tissue damage characteristic of percutaneous ethanol injection, owing to the uneven distribution of ethanol within the tissue, suggests that ILP might be useful in the ablation of thyroid malignancies. Although our statistical analysis showed an initial linear correlation between output power and delivered energy and the size of the laser-induced lesion, for the highest values of power and delivered energy used in our model, curves show a plateau that suggests logarithmic behavior.

The advantage of laser as compared with other modes of energy delivery is the great precision of laser-induced necrosis (9). However, maintenance of light penetration during laser treatment is a prerequisite for controlled and predictable tissue heating. Determining the volume of the treated area is complex: it depends on laser power, laser irradiation time, wavelength of light involved and how it reaches the tissue, and tissue factors such as optical and thermal characteristics (9,12,15,19). As different types of tissue have different optical properties, the effect of a specific laser treatment will vary in accordance with the tissue type involved (12,15). Further experimental and clinical data are needed for a thorough understanding of the relationship between tissue temperature and the quantity of laser energy applied (9,19).

At US monitoring, the fiber tip was always clearly depicted as a hyperechoic spot, and during laser irradiation as an irregular hyperechoic area enlarging over time. Real-time imaging of the treated areas was reported as reliable in predicting the extent of ILP damage in the treatment of small hepatic lesions (11,15,18). However, in our study, as well as in previous studies (14,21,22), the size of the hyperechoic zone served only as a rough guide to the extent of necrosis, and no correlation (r = 0.11; P = .085) was found between the actual laser-induced lesions and US images. Therefore, therapeutic use of ILP appears to be hazardous for the ablation of cervical lesions in clinical practice.

Magnetic resonance imaging guidance is reported to provide clear and accurate monitoring of laser-induced tissue damage in the treated area in experimental models and in clinical studies (12,20), but it is time-consuming and expensive and cannot be used to predict final necrosis volume as does US (24,25). Moreover, the presence of large colloid or fluid collections prevents heat diffusion within the tissue. This physical phenomenon could sharply and unpredictably reduce the effectiveness of ILP treatment in cystic tumors.

Findings in our feasibility study suggest that US can be used for locating target thyroid lesions, guiding interstitial optical fiber insertion, and monitoring the development of thermal necrosis. ILP treatment in itself appeared feasible and unproblematic. US-guided needle insertion into autonomously functioning thyroid nodules was performed easily according to the procedure described for percutaneous ethanol injection (1,2). The narrow width of the optical fiber made use of fine needles possible, which prevented local discomfort, so only mild local anesthesia was needed. Laser firing induced a mild burning sensation, reportedly no more painful than fine-needle aspiration biopsy. No damage was induced along the needle track or at the skin surface.

ILP could be a therapeutic tool for highly selected problems in thyroid tumor treatment. However, still unresolved problems that currently complicate the practical application of laser ablation of thyroid tumors are as follows: (a) The correlation of US with the volume of necrosis is often unpredictable. The difficulties in mapping the exact margin of the treated tumor make it possible to perform only a debulking and not a complete destruction of neoplastic lesions of the thyroid. Since the most important improvement in the technique would involve a real-time US prediction of the actual extent of thermal necrosis during laser firing, power Doppler evaluation of the thyroid gland during laser illumination could be used to show the absence of blood flow within the tissue that has undergone coagulative necrosis. However, this is feasible only after cessation of the interference caused by laser firing. (b) The volume of ablated tissue is limited. To debulk substantial tumor volumes, multiple fibers must be used. (c) There are vital surrounding structures in the neck. The contiguity of laryngeal nerves, carotid arteries, and the upper airway make it impossible to place laser margins beyond the tumor to ensure complete ablation of large neoplastic lesions within the thyroid gland. (d) The presence of cavitary areas, colloid collections, and necrotic and hemorrhagic changes leads to differences in heat dispersion within the tumor. Therefore, some tumors may be more responsive to this type of therapy than are others. (e) Central scarring and cavitation create problems in the use of lasers for ablating tissue. Therefore, cavitation and charring should be avoided by using a low-energy laser for prolonged periods.

Because of these difficulties, a more useful initial laser application in humans might be in the treatment of benign thyroid nodules, in which debulking alone may help alleviate the problem. As in the present study, in vivo treatments were attempted only to test the feasibility and safety of the procedure. Further studies are needed to assess the interference caused by the role of circulating blood in laser-induced thyroid damage.


   FOOTNOTES
 
Abbreviation: ILP = interstitial laser photocoagulation

Author contributions: Guarantor of integrity of entire study, C.M.P.; study concepts, C.M.P., G.B., E.P.; study design, C.M.P., G.B., S.P., E.P.; definition of intellectual content, C.M.P., G.B., E.P.; literature research, R.G., C.M.P., E.P.; clinical studies, E.P., R.G.; experimental studies, A.C., G.B., A.B., C.M.P.; data acquisition, A.B., S.P., V.A.; data analysis, C.M.P., G.B., R.G., A.B.; statistical analysis, R.G., A.B.; manuscript preparation, R.G., A.B., V.A., A.C., S.P.; manuscript editing, A.B., S.P.; manuscript review, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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  7. Livraghi T, Paracchi A, Ferrari C, Reschini E, Macchi RM, Bonifacino A. Treatment of autonomous thyroid nodules with percutaneous ethanol injection: 4-year experience. Radiology 1994; 190:529-533.[Abstract/Free Full Text]
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  9. Matthewson K, Coleridge-Smith P, O’Sullivan P, et al. Biological effects of intrahepatic neodymium:yttrium-aluminium-garnet laser photocoagulation in rats. Gastroenterology 1987; 93:550-557.[Medline]
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  19. Nolsøe CP, Torp-Pedersen S, Burchart F, et al. Interstitial hyperthermia of colorectal liver metastases with a US-guided Nd:YAG laser with a diffuser tip: a pilot clinical study. Radiology 1993; 187:333-337.[Abstract/Free Full Text]
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F N Bennedbak, S Karstrup, and L Hegedus
Ultrasound guided laser ablation of a parathyroid adenoma
Br. J. Radiol., October 1, 2001; 74(886): 905 - 907.
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