Ultrasound-guided, minimally invasive therapy for recurrent head and neck carcinomas

ULTRASOUND-GUIDED, MINIMALLY INVASIVE THERAPY FOR RECURRENT HEAD AND NECK CARCINOMAS

DAN J. CASTRO, MD, THOMAS CALCATERRA, MD, ROMAINE E. SAXTON, PhD, ROBERT LUFKIN, MD, MARCOS PAIVA, MD, JENNINE ALDINGER, RDMS, JACQUE SOUDANT, MD

Imaging-guided, minimally invasive surgery is a new concept that uses ultrasound (US) and/or high-speed magnetic resonance imaging (MRI) to guide various energy sources such as lasers, radio frequency, ultrasonic, or cryotherapy devices for treatment of deep-seated tumors and to monitor tissue changes during energy deposition. This approach for treatment of cancer will become clinically useful only after development of high resolution methods for real time monitoring of energy deposition in tumors. Recent studies have shown the efficiency of US and MRI for real and/or near real time tumor and vessel identification as well as for monitoring and quantifying energy-induced tissue damage. We report our initial clinical experience with patients in whom US and/or MRI-guided interstitial tumor therapy (ITT) techniques were successfully applied for the treatment of recurrent, nonresectable, local, and/or metastatic head and neck carcinomas. Patients were treated on an outpatient basis either in the operating room or in an upgraded, specially equipped SIGNA 1.5 T magnetic resonance suite. Most patients tolerated these procedures well and were successfully palliated for periods ranging from 3 months to 6 years posttreatment. The clinical experience and steps that led to our current technique are reviewed.

The failure rate in the treatment of advanced head and neck carcinomas remains unacceptably high despite surgery, radiation, and/or chemotherapy. One third to one half of all stage III and/or stage IV cancer patients develop persistent or recurrent disease within the first 5 years. 1 Survival rates for head and neck cancers recurrent after primary treatment are very poor. Nearly all of these patients die within 1 year, usually with severe functional and cosmetic problems. 2

Recent changes in health care policies have lead to drastic pressures on physicians to reduce cost while im- proving quality. The technological revolution of the last decade in the fields of optics, electronics, computers, and software have facilitated the evolution of minimally invasive techniques with reduced morbidity and disability.

Imaging-guided interstitial tumor therapy (ITT) is a new and promising clinical alternative that has recent-

From the Department of Head and Neck Surgery, Department of Radiological Sciences, Division of Surgical Oncology, UCLA School of Medicine, Los Angeles, CA; Department of Head and Neck Sur- gery, Groupe Hospitalier Pitie-Salpetriere, Paris, France.

Supported by the Association de Recherche sur le Cancer Grant No. A.R.C., BP 3-94801 Villejuif Cedex, France, Division of Head and Neck Surgery; the Jonsson Comprehensive Cancer Center CICR Award; University of California Los Angeles School of Medicine; Na- tional Institutes of Health Grant No. USHHS DC 00031 ; E-Z-EM, Inc; Laserscope, Resonance Technology, Inc; In Vivo Research Inc; Oh- meda Inc; GE Medical Systems; and The George Spota Memorial Fund.

Address reprint requests to Dan J. Castro, MD, Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, CA 90024- 1624.

Copyright �9 1994 by W.B. Saunders Company 1043-1810/94/0504-0005505.00/0

ly been s h o w n to be safe and cos t -e f fec t ive . 3-6 Ultrasound (US) and/or high-speed magnetic resonance imaging (MRI) are used to delineate the underlying anatomy and help guide and monitor tissue changes during energy deposition in tumors. 7 During the last 6 years a series of 55 patients with recurrent, unresectable head and neck carcinomas were treated using this technique. Most patients were successfully palliated, with a prolonged median survival rate of 18 months. The steps that led to our current technique and future perspectives are described.

PATIENTS AND METHODS

From 1988 to 1994, 55 patients with advanced cancer were treated using imaging-guided therapy at the University of California Los Angeles (UCLA). All patients presented with either recurrent and/or metastatic unresectable tumors that had not responded to previous surgery, radiation therapy, chemotherapy, hyperthermia, and other treatment modalities. The age distribution of the reviewed cases ranged from 45 to 88 years, with a peak incidence in the fifth and sixth decade. There were 36 men (65%) and 19 women (35%) in this cohort. All patients presented with one to four recurrent tumors. One to 12 palliative sessions of imaging-guided surgery were performed on the patients, with a mean of four treatments. The survival ranged between 3 months to 5 years posttreatment with a mean of 18 months. The an- atomic locations of these tumors are summarized in Table 1, with most occurring in the head and neck area.

Most patients (70%) presented with pain as their major complaint. However, others presented with associated

OPERATIVE TECHNIQUES IN OTOLARYNGOLOGY--HEAD AND NECK SURGERY, VOL 5, NO 4 (DEC), 1994: pp 259-266 259

TABLE 1. Imaging-Guided Therapy: Tumor Locations in Study Group

Location Number

Base of skull 2 Base of tongue 3 Buccal mucosa 5 Floor of mouth 7 Lateral tongue 3 Lateral pharyngeal wall 2 Maxillary sinus 2 Nasopharynx 2 Neck 10 Nose 2 Palate (hard and soft) 3 Posterior pharynx 1 Subcutaneous 4 Tracheobronchial tree 9

dysphagia, dyspnea, bleeding, difficulties chewing and/ or swallowing, and/or cosmetic deformities. Most patients were subjected to a routine of clinical evaluations that included preoperative MRI, US, or positron emission tomography (PET) studies to assess the anatomy, tumor location, volume, underlying vascular supply, and met- abolic activity. Tumor volume ranged from 2 to 80 cm 3, with a mean of 35 cm 3. Diagnosis was confirmed in all patients through biopsy. The histology was predomi- nantly squamous cell carcinoma (90%), but included mel- anoma, adenocarcinoma, medullary thyroid carcinoma, adenoma, angiosarcoma, and chondrosarcoma.

TECHNIQUE

Procedures were performed in the operating room on an inpatient or outpatient basis. After obtaining appropri- ate informed consent, the patients were placed on continuous cardiac and pulse oximetry monitoring and then heavily sedated or placed under general anesthesia. The surgical field was prepped and draped in a sterile fashion, and the skin overlying the tumor mass was anes- thetized with 1% lidocaine with 1:100,000 epinephrine. A variable number of 16-g angiocath or E-Z-EM (E-Z-EM, Inc, Westbury, NY) needles with a suction port were then passed percutaneously into the tumor mass when interstitial treatment was performed: US was used in 50 patients to confirm the position of the tip of the catheters within the tumor mass, with special attention given to the proximity to larger vessels and tumor neovascularity. The first five patients (3,5,6) were treated in the upgraded 1.5 T interventional MRI unit (GE Medical Systems, Mil- waukee, WI) equipped with a treatment monitoring system.

The 600-~m flexible Nd:YAG laser fiberoptic cable was then passed through the needle lumen and into the tumor mass. Nd:YAG laser energy was applied interstitially and/or externally, guided by US as a monitoring technique to 90% of the patients. In the last eight patients (15%) ultrasonic energy delivery was used first, either externally and/or interstitially, to rapidly debulk the tumor, then the tumor bed was treated with the Nd:YAG laser.

RESULTS

A series of 55 patients were treated over a 6-year period at UCLA School of Medicine, using several approaches of imaging-guided, minimally invasive therapy. All pa-

tients presenting with recurrent, unresectable tumors had not responded to previous conventional therapy. Most patients were in their fifth and sixth decade of life and were considered for palliation in an attempt to control symptoms such as pain, dysphagia, dyspnea, and bleeding. The majority of treated tumors (90%) were treated in the operating room using US as the guiding imaging modality, whereas 9% were treated in the interventional MRI suite. In 90% of the cases the Nd:YAG laser was used either externally and/or interstitially to photablate the tumors, whereas the ultrasonic energy was used in the later cases in conjunction with the Nd:YAG laser. Nearly all patients (90%) were treated on an outpatient basis with 80% showing improvement and/ or resolution of symptoms after one to five sessions, with a mean of two treatments. In 70% of the patients, local tumor control or cure was observed.

This response was inversely related to the initial tumor volume and was dependent on histology and growth rate. Smaller, slow growing, more differentiated tumors were palliated successfully and had a better local cure rate than rapidly dividing malignancies. Over 80% of the patients showed significant functional and/or cosmetic improvement and were able to resume daily activities for periods of up to 5 years posttreatment, with a mean of 18 months. One major complication was observed in the second patient treated under MRI guidance. Periopera- tive bleeding noted during interstitial laser energy deposition required embolization and intubation for airway protection. This patient did well afterward and is still alive at 4 years posttreatment. The first patient treated was the only one to die within 3 months postoperatively (of unrelated cardiopulmonary disease); the others had a mean survival of 18 months.

DISCUSSION

This first use of heat for destruction of tumors dates back to 1700 BC. Breasted describes treatment of tumors on the breast using the glowing tip of a firedrill, s Classical Greek and Roman cultures used heat widely as a therapeutic tool, and its combination of homeostatic and tissue-destro~fing properties was regarded as particularly valuable. ~ Total b o d y hyper the rmia , us ing fever- inducing infections, as a primary or adjuvant treatment of

lo cancer was based on original observations by Busch in 1 1 1866 and later by Coley. A number of cures of sarco-

mas and other tumors were reported. 1~ King et al, 12 during the 1940s, described the effects of hyperthermia on the liver of patients undergoing treatment for resistant gonococcal and nonspecific urethritis. Jaundice developed in 10% to 20% of the patients and all had abnormal liver funct ion. The pa tho logy of those w h o died showed inflammatory and scattered necrotic changes. 13 Recovery and survival were associated with the gradual return to normal of liver function and normal histology results on liver biopsy. 14

A number of methods of inducing hyperthermia have been tested, including electromagnetic waves (radiofrequency and microwave), whole body heating by external and extracorporeal means, and ultrasound. Wills et a115 and Quebbeman et a116 found no advantages to whole body hyperthermia and reported a 24% mortality rate.

17 Storm et al and Baker et al ~s recently tested regional radiofrequency hyperthermia for treatment of liver and pancreatic tumors with some evidence of subjective improvement but minimal evidence of prolonged survival.

260 US-GUIDED THERAPY FOR HEAD AND NECK CARCINOMAS

Complications included skin and subcutaneous fat burns (7% to 12%). Technical problems 17"18 were also observed in measuring, achieving, and maintaining the de- sired therapeutic temperatures throughout the tumor.

Another method for inducing local necrosis of liver tumors is cryotherapy, applied to the surface or interstitially, which was tested by Ravikumar et a119 and Zhou et al. 2~ Tumor eradication has been reported in some cases and survival times for patients with otherwise untreat- able tumors were increased. Dritchilo et a121 recently reported that interstitial implantation of radioactive seeds in tumors caused tumor necrosis, but the effect on survival is not yet clear. Livraghi et a122 and Shiina et a123 have injected, under ultrasound guidance, 95% alcohol into the center of tumors to induce tumor necrosis with few complications. However, this approach was rather imprecise in its administration and prediction of effect. Clearly these techniques are not ideal. Cryotherapy re- quires a laparotomy for application, which limits repeated treatments, and alcohol injection is limited in pre- cision, with a need for repeated injection on many occa- sions. US- and/or MR-gu ided intersti t ial t he rapy accomplishes tumor necrosis in a predictive way, delivered via minimally invasive access and real time monitoring systems to avoid undesirable damage to adjacent normal tissues.

ITT is a promising new approach for ablation of head and neck tumors, because it is minimally invasive and allows precise and controlled delivery of photothermal energy into t i ssues . 3-5'24-32 However, ITT will become clinically useful only when real time, noninvasive, and reproducible methods to monitor energy delivery to tissues and/or the tumor ablation process are developed. Invasive methods currently available use thermal probes, infrared thermography, and histological studies, 33"34 which are reliable but have limited clinical applications. Since the mid-1970s, interstitial placement of laser fi- beroptics has been applied successfully for treatment of large subcutaneous metastasis. 35 Svaasand et a136 reported preliminary optical dosimetry for interstitial phototherapy of malignant tumors. Brown 37 investigated the interstitial treatment with the Nd:YAG laser for hepatic hyperthermia in a number of applications. Mat- thewson et a138 tested a single Nd:YAG laser for hepatic hyperthermia in a number of applications. Matthewson et a138 tested a single Nd:YAG laser fiber at low power (1 or 2 W) to produce areas of thermal necrosis of 16 to 11 mm at great speed in the porcine liver. However, the high-power density at the distal end of the fiberoptic re- sulted in frequent tip damage, with burning and nonuni- form distribution of laser energy, leading to poorly reproducible tissue effects.

Daikunozo and Joffe 39 further developed a computer- controlled Nd:YAG system for interstitial local hyperthermia. To increase the area of tissue necrosis produced by the laser, Steger and Bown 4~ used fiberoptic coupling systems and increased the number of fibers transmitting laser energy. This concept is attractive but has been dif- ficult to achieve in practice.

During the last 6 years, our approach for imaging- guided palliative therapy of head and neck tumors has evolved, and multiple steps have led to our current technique. A conservative approach was initially used, with the 1.06-~m Nd:YAG laser implanted interstitially in tumors. In the first 15 patients treated, care was taken to photoablate only a small and limited volume of tumor during each treatment, while leaving ample margins of untreated tumor behind, because no experience was

available and the side effects were unknown. Only one needle was implanted in the center of the tumor, and after confirmation of its position with the US, a 600-mm flexible Nd:YAG laser fiberoptic was inserted. The Nd:YAG laser was set at 25 W in a continuous mode. A total of four Nd:YAG laser exposures, each lasting 15 seconds, were delivered to the center of the tumor, while the transient hyperechoic signal generated during energy deposition was monitored with the US. Between each laser exposure, the Nd:YAG laser fiber was removed and its tip cleaned and reshaped. These patients tolerated the treatments well and the only side effect observed was a transient postoperat ive increase in tumor volume caused by edema. No infections occurred; however, most of these patients required multiple treatment sessions (up to 12 times) to completely control these tumors. The number of treatment sessions was linearly related to the original tumor volume and its rate of regrowth. Smaller and slow-growing tumors required the least number of sessions. However, a number of problems were identified in the first 15 patients treated. First, there was a transient (2-week) postoperative increase in tumor volumes that was accompanied by worsening of the symptoms (pain, swelling). These symptoms improved later, when the tumor volume decreased.

Second, because no cooling of the Nd:YAG laser fiber was used during energy deposition, the laser tip was fre- quently damaged, and it had to be cleaved and reshaped multiple times during each procedure.

Third, only one major complication occurred in the second patient who was treated under MRI guidance in 1990. Perioperative bleeding noted during interstitial Nd:YAG laser energy deposition required embolization and 24-hour intubation for airway protection. This patient did well afterward and is still alive 4 years after treatment, with no evidence of a local recurrence. This complication was caused by a poor technique of needle tip localization under MRI guidance. This problem has been resolved since then with the use of US for real time needle introduction and localization and the availability of faster MRI pulse sequences.

Fourth, too many treatment sessions were required to achieve local tumor control. An average of eight treatments was required per patient to notice significant improvement of symptoms. Patients were treated every 2 to 4 weeks, and during each treatment only a small and limited volume of the residual tumor was destroyed.

To reduce the number of treatments per patient, and avoid potential bleeding complications and damage to the Nd:YAG laser fiber tip during energy deposition a number of changes were tested in the next five patients. First, all patients were scanned with a color Doppler US preoperatively to map the underlying tumor vasculature and its relationships with surrounding major blood vessels. All patients with tumors surrounding the carotid artery in the neck and/or base of skull area were excluded from our study early on. However, two patients in the last 6 months with base of skull and carotid artery in- volvement were successfully palliated after carotid artery occlusion followed by US-guided ultrasonic/Nd:YAG laser excision.

Second, an irrigation/suction system was added, using normal saline during interstitial Nd:YAG laser energy deposition. This measure has significantly reduced the frequency of damage to the fiber's tip and prevented charred tissue from accumulating around the fiber.

Third, an attempt to photoablate a larger volume of tumor during each treatment was made by inserting mul-

CASTRO ET AL 261

tiple needles at various sites of the tumor under US guidance. Each site was then treated separately with interstitial Nd:YAG laser energy while monitoring its effects with US. The largest tumor treated in one session was of 40 cm 3, as measured by preoperative MRI. This tumor was a poorly differentiated squamous cell carcinoma located at the level of base of skull. Interestingly, this patient did well postoperatively, with no significant side effects except for a large amount of necrotic debris that drained from all the needle sites at 2 weeks after treatment. No other side effects were noted, despite the fact that only oral antibiotics were administered. This patient is still alive at 4 years after surgery, with no evidence of a local recurrence. However, the patient recently developed a malignant pleural effusion and is currently undergoing 5-fluorouracil chemotherapy. The other patients treated using this technique did well except for a transient (2- to 4-week) increase in their symptoms (pain, swallowing difficulties).

It was noted that the clinical symptoms were propor- tionally related to the changes in tumor volume. There- fore, to rapidly debulk tumors during each treatment, in addition to the measures previously described, an attempt was made to suction all the debris. This proved to be more effective and symptoms such as pain and swallowing rapidly improved postoperatively (1 to 3 days). This technique seemed to be safe and effective because no major complications occurred when it was tested on 15 patients with head and neck recurrences between 4 to 50 cm 3. Howeve r , the p rocedure time seemed to be lengthy, with an average operating time of 2 hours, because the Nd:YAG laser was the only source of energy used for tumor eradication.

To reduce the operating time for the last patients treated for tumors >20 cm 3, the CUSA ultrasonic/RF surgical aspirator (Fig 1, Valley Lab, Boulder, CO) was used in conjunction with the Nd:YAG laser, irrigation/suction

FIGURE 1. Ultrasound-guided interstitial ultrasonic (CUSA) aspiration of a recurrent, unresectable pre-parotid/base of skull squamous cell carcinoma. The facial nerve was previously surgically removed.

FIGURE 2. After debulking the tumor with the ultrasonic aspirator (Fig 1), the 1.06-~m Nd:YAG laser is inserted interstitially. The tumor bed is then treated with the Nd:YAG laser while monitoring its effects with the US.

systems (Figs 2, 3, 4). For accessible and large tumors, the ultrasonic aspirator is now used to rapidly debulk the treated tumor, while the interstitial Nd:YAG laser with suction/irrigation is used to treat the underlying bed and margins. The operating time is reduced to 45 minutes and all patients are doing well.

Tumors located in the oral cavity, pharynx, hypophar- ynx, larynx, and esophagus were treated endoscopically with the Nd:YAG laser fiber mounted on a fraiser suction catheter, while the 10-MHz US transducer is placed externally on the neck, monitoring the underlying anatomy, vascular supply, and treatment effects (Figs 5 and 6).

To avoid the possibility of tumor-cell seeding along the path of the needles during insertion and/or extrusion, new needles were used for each passage. In addition, the Nd:YAG laser remained powered while the needle was removed from the target. In all of our patients treated, no evidence of recurrences and/or tumor regrowth along the needle's p a t h w a s noted.

Gatenby et a141 tested computerized tomography (CT)- guided laser therapy for treatment of resistant tumors in 10 patients with favorable results. Steger et a142 used ultrasound imaging to monitor the percutaneous interstitial Nd:YAG laser treatment of 10 patients with liver tumors and 3 with pancreatic cancer. Results of these studies show that growth of the laser-treated tumors can be arrested or reduced after treatment, but overall survival was not affected.

Steger et a142 found ultrasound imaging to be a sensi- tive monitoring technique for thermal necrosis of the liver. However, Dachman et a143 reported ultrasound- detected laser-induced changes mainly consistent with cavitation. Previous studies showed that an energy density of at least 12,000 J/cm 2 of the Nd:YAG laser is needed (400-~m fiber, 4 W, 6 minutes) to visualize cavitation with ultrasound, as opposed to energy density as low as 1,250

2 6 2 US-GUIDED THERAPY FOR HEAD AND NECK CARCINOMAS

FIGURE 3. Postsurgical view of the patient shown in Fig 1. Note the resolution of the pre-parotidfoase of skull tumor.

FIGURE 4. Ultrasound-guided interstitial Nd:YAG laser treatment of a parapharyngeal tumor. FIGURE 5. Ultrasound localization of the laser needle tip of

patient shown in Fig 4. Note the proximity to the vessel.

J/cm 2 for MRI. 3 However, at energy densities as low as 300 J/cm 2, a transient hyperechoic signal is seen, using real time ultrasound during Nd:YAG laser energy deposition in tissues. Recent studies 44 in bovine liver ex vivo showed a linear relationship between interstitial Nd:YAG laser energies (300 to 1,200 J cm2), transient hyperechoic US signal changes, and histology. However, use of ultrasound in the skull base and other bony region areas may have limited applications because of the high reflec- tion of the beam.

Previous ultrasound applications have been used with the Nd:YAG laser to guide vaporization of liver metastasis w h e n formal resect ion is no longer possible. 45

Endoscopic ul t rasonography also has been used for Nd:YAG laser palliation of gastrointestinal carcinomas to define tumor thickness and decrease the risk of perfo- ration. In a pilot study, 44 intraoperative ul trasound technology was used to define the vascular anatomy of advanced head and neck cancer, thus reducing morbidity from hemorrhage during laser palliation. During laser illumination (Fig 7), a hyperechoic image is produced that is thought to result from boiling of tissue water and the local production of vapor bubbles (Fig 8). 44 These changes are observed with respect to the visible tumor margins and adjacent blood vessels to achieve maximal safe tumor destruction while limiting the risk of bleeding.

CASTRO ET AL 263

FIGURE 6. Ultrasound-guided interstitial Nd:YAG laser therapy of a recurrent submental squamous carcinoma. Note the channels for the laser and for aspiration.

The first five patients with recurrent, unresectable head and neck tumors were treated in a standard MRI suite and later in an upgraded 1.5 T MRI suite. 6 Because our initial experimental results 1-12 showed a high sensitivity and linear relationship 3-5"24-32 between the measured MRI signal intensity change, the amount of interstitial energy deposition in tissues, and histological damages, the de- cision to use MRI as the guiding modality for this technique was made. However, the average procedure time in the MRI interventional suite lasted between 3 to 5 hours because of the slow technique of needle localization and difficulties in monitoring blood flow. Further- more, the cost of upgrades to this MRI interventional suite exceeded $500,000, and its accessibility to patients

was still limited. Therefore, we elected to use color Doppler ultrasonography for the last 50 patients treated, because it is portable, easily adaptable to the operating room, and cost-effective. In addition, so far, US has been found to be the most practical imaging modality for real time guidance and localization of interstitial needles and/or probes in a target.

Because color Doppler ultrasonography is currently the most useful modality for noninvasive monitoring of blood flow, its use during the procedure has helped us to avoid any further bleeding complications.

Before treatment, a tumor appears as a zone of hypoechoic signal on US, which completely regresses after successful debulking with interstitial ultrasonic energy, followed by Nd:YAG laser photoCoagulation of the tumor bed.

CONCLUSIONS

This study reviews a series of 55 patients with unresectable, recurrent head and neck malignancies successfully palliated over the last 6 years by imaging-guided, minimally invasive laser therapy. Intraoperative color-flow Doppler ultrasonography and MRI have become useful monitoring techniques for the clinical application of interstitial energy deposition in patients with advanced head and neck cancer. Ultrasound is particularly useful because it generates real time images, is readily adapted to the operating room, and accurately depicts vascular anatomy. The techniques developed for Nd:YAG laser with or without ultrasonic ITT may be adaptable to other forms of minimally invasive ITT, using lasers of other wavelengths, radiofrequency devices, microwaves, cryotherapy, ethanol injection, or interstitial radioactive seed implantation. Such treatments have the potential to provide meaningful palliation for patients with advanced head and neck cancer on a cost-efficient, outpatient basis.

FIGURE 7. Ultrasound needle tip localization in the tumor of the patient shown in Fig 6. The tumor generates a hypoechoic signal on ultrasound.


F I G U R E 8. A t rans ient hype recho ic signal is s h o w n on u l t r a sound whi le the N d : Y A G laser remains p o w e r e d .

ACKNOWLEDGMENT We wish to thank Jeanet te Infield for he r technical suppor t .

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Ultrasound-guided, minimally invasive therapy for recurrent head and neck carcinomas

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