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DOI:10.2214/AJR.05.0804
AJR 2006; 187:W333-W340
© American Roentgen Ray Society

Original Research

Intraoperative Triple Antenna Hepatic Microwave Ablation

Caroline J. Simon1, Damian E. Dupuy1, David A. Iannitti2, David S. K. Lu3, Nam C. Yu3, Bassam I. Aswad4, Ronald W. Busuttil5 and Charles Lassman6

1 Department of Diagnostic Imaging, Brown Medical School, Rhode Island Hospital, 593 Eddy St., Providence, RI 02903.
2 Department of Surgery, Brown Medical School, Rhode Island Hospital, Providence, RI.
3 Department of Diagnostic Imaging, David Geffen School of Medicine at UCLA, Los Angeles, CA.
4 Department of Pathology, Brown Medical School, Rhode Island Hospital, Providence, RI.
5 Department of Surgery, David Geffen School of Medicine at UCLA, Los Angeles, CA.
6 Department of Pathology, David Geffen School of Medicine at UCLA, Los Angeles, CA.

Received May 11, 2005; accepted after revision August 12, 2005.

 
This research was sponsored in part with a grant from Vivant Medical Inc., Mountain View, CA.

Address correspondence to D. E. Dupuy (ddupuy{at}lifespan.org).

WEB

This is a Web exclusive article.


Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. Microwave ablation is emerging as a new treatment option for patients with unresectable hepatic malignancies. This two-center study shows the results of a phase 1 clinical trial of patients with known hepatic masses who underwent synchronous triple antenna microwave ablation before elective hepatic resection.

SUBJECTS AND METHODS. Intraoperative microwave ablation was performed before hepatic resection. Hepatic lesions were targeted using real-time intraoperative sonography with three microwave antennas positioned in a triangular configuration. Microwave ablation was performed at 45 W for 10 minutes. Hepatic resection was then completed in the standard fashion. Gross specimens were sectioned and measured to determine tumor and ablation sizes. Representative areas were stained with H and E stain and vital histochemical nicotinamide adenine dinucleotide (NADH) stain.

RESULTS. Ten patients with a mean age of 64 years (range, 48-79 years) were treated. Tumor histology included colorectal carcinoma metastases and hepatocellular carcinoma. The mean maximal tumor diameter was 4.4 cm (range, 2.0-5.7 cm). The mean maximal ablation diameter was 5.5 cm (range, 5.0-6.5 cm), while the average ablation zone volume was 50.8 cm3 (range, 30.3-65.5 cm3). Gross and microscopic examinations of areas after microwave ablation showed clear coagulation necrosis, even surrounding large hepatic vessels (> 3 mm in diameter). A marked thermallike effect was observed with maximal intensity closest to the antenna sites. NADH staining confirmed the uniform absence of viable tumor in the ablation zone.

CONCLUSION. This study shows the feasibility of using multiple microwave antennas simultaneously in the treatment of liver tumors intraoperatively. Additional percutaneous studies are currently under way to investigate the safety and efficacy in treating nonsurgical candidates.

Keywords: liver metastases • microwave ablation • radiofrequency ablation • radiologic-pathologic correlation


Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
Hepatic tumors, whether primary or secondary in nature, remain a difficult management challenge for all clinicians. In 2005, it was predicted that there would be more than 667,000 new cases of liver cancer throughout the world with more than 17,000 of the cases occurring in the United States alone [1]. The most common type of primary liver cancer is hepatocellular carcinoma (HCC), making it one of the most prevalent and fatal of all malignancies. Although its incidence in the United States continues to rise, only up to a third of patients are suitable candidates for hepatic resection at the time of presentation [2]. In addition, of the estimated 145,000 new cases of colorectal cancer in the United States in 2005, 25% of these patients will have underlying metastatic disease at the time of clinical presentation, with an additional 20-25% developing metastases within a 5-year interval [1]. Again, only a minority (10-20%) of these patients with hepatic colorectal carcinoma (CRC) metastases will be candidates for liver resection [1].

Given the unresectability of most liver neoplasms at the time of diagnosis, local thermoablative techniques have been widely researched and integrated into the treatment and management of these patients.

In 2003, a new microwave ablation system was engineered in the United States [3]. Advances incorporated into this system included the specific tuning of microwave antennas to the dielectric properties of liver tumors, thus reducing feedback while increasing the amount of energy deposited in the surrounding tissues. In vivo experimentation with porcine liver using triple antenna ablation produced synergistically larger ablation lesions [4] than those produced by single antenna ablation, thus hinting at the more convenient and effective treatment of large tumors using microwave ablation. A novel microwave loop antenna has also been studied in the single and double (parallel and orthogonal) configurations with reports of precise and effective targeting in in vivo porcine tissue [5].

In this article, we report our ablate and resect observations with pathologic correlation using this new microwave ablation device with a triple straight antenna design to treat liver tumors. Specifically, our primary aim was to evaluate the size and microwave ablation characteristics in both hepatic neoplasms and the adjacent normal liver parenchyma.


Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Patient Population
This was a joint study performed at two tertiary cancer treatment centers in the United States. The prospective study was approved by the respective institutional review boards. From May 2003 to January 2004, 20 patients with liver masses who were to be scheduled for curative liver resection were identified and subsequently enrolled in this ablate and resect study. Ten patients underwent microwave ablation with the triple antenna configuration and were included in this study. Relevant patient exclusion criteria included patients who had lesions ablated using single or double microwave antenna configurations and a patient diagnosed with focal nodular hyperplasia. Additional patient and tumor characteristics are summarized in Table 1.


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  		TABLE 1: Patient and Tumor Characteristics with Ablation Zone Sizes

 

Informed consent was obtained from all the patients. The patient population consisted of an equal number of men and women with a mean age of 64 years (range, 48-79 years). All patients had undergone either multiphase CT or gadolinium-enhanced MRI to delineate the target tumor and to assist with surgical planning. The initial diagnosis of liver malignancy was based on preoperative tissue biopsy, classical imaging characteristics of tumor hypervascularity, or both and was correlated with the relevant clinical and surgical history of the patient.

Microwave Ablation System
The microwave ablation system used was the VivaWave Microwave Coagulation System (Vivant Medical). Three microwave generators were used, each capable of producing up to 60 W of power at a frequency of 915 MHz. Each generator was connected to a microwave antenna using a coaxial cable. The three single microwave antennas were then arranged in a three-probe triangular clusterlike configuration, spaced (using a rigid spacer supplied by the manufacturer) at 1.5 cm (n = 3), 2.0 cm (n = 6), and 2.5 cm (n = 1). These straight microwave antennas had a 13-gauge diameter, 15-cm length, and 3.6-cm active tip (Fig. 1).


Figure 1
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  		Fig. 1 —Photograph shows single straight microwave antenna (VivaTip Surgical, Vivant Medical) with 3.6-cm active tip.

 
Microwave Ablation Treat and Resect Protocol
All microwave ablations were performed intra-operatively under sonography guidance. All operations were performed with the patient under general anesthesia, and exposure of the targeted hepatic lobe was performed in the standard fashion by a hepatobiliary surgical team. Intraoperative hepatic sonography was then performed by the attending radiologist. In a systematic manner, the location and size of the index tumor identified on preoperative CT or MRI were reconfirmed, and the rest of the liver was scanned to ensure the presence or absence of any other suspicious masses. The microwave antennas were placed into the center of the index tumor under direct sonography guidance (Fig. 2). All three microwave generators were powered on simultaneously to achieve synchronous ablation. All ablations were performed at a power of 45 W for a treatment period of 10 min. Each patient underwent a single microwave ablation for their solitary liver cancer (either HCC or CRC metastasis). Continuous sonography monitoring was performed to track the progress of the ablation (Figs. 3A, 3B, and 3C).


Figure 2
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  		Fig. 2 —Digital photograph of 48-year-old woman with colorectal carcinoma metastases taken intraoperatively shows insertion of three single microwave antennas (VivaWave Microwave Coagulation System, Vivant Medical) spaced 2.0 cm apart using rigid spacer.

 

Figure 3
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  		Fig. 3A —48-year-old woman with colorectal carcinoma metastases (patient 1 in Table 1). Sequential sonograms (taken 1-2 minutes apart) show development of exuberant transient hyperechogenic response in surrounding liver parenchyma to microwave ablation.

 

Figure 4
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  		Fig. 3B —48-year-old woman with colorectal carcinoma metastases (patient 1 in Table 1). Sequential sonograms (taken 1-2 minutes apart) show development of exuberant transient hyperechogenic response in surrounding liver parenchyma to microwave ablation.

 

Figure 5
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  		Fig. 3C —48-year-old woman with colorectal carcinoma metastases (patient 1 in Table 1). Sequential sonograms (taken 1-2 minutes apart) show development of exuberant transient hyperechogenic response in surrounding liver parenchyma to microwave ablation.

 
The extent of the ablated coagulation "front" could be roughly approximated on the basis of the appearance of the transient hyperechoic zone. In the case of radiofrequency ablation, the transient hyperechoic response is said to be a rough approximation (± 8 mm) of the ablation margin [6]. With microwave ablation, however, the echogenic response observed was more rapid and extensive, making visualization of the antenna and ablation zone slightly more difficult. Therefore, response is not as useful with microwave ablation as compared with radiofrequency ablation. Also of note was the fact that the transient hyperechoic zone exhibited an exuberant and robust response, as previously reported by Wright et al. [4], thus suggesting the high intratumoral temperature achieved. Immediately after ablation, targeted hepatic resection was completed by a surgical team. The Pringle maneuver was not used in this study (although larger ablation volumes would be expected with this maneuver than without this maneuver) because one of the long-term goals of our study is to make the data set as applicable to the percutaneous setting as possible.

Pathologic Correlation
The resected hepatic specimen, which contained the tumor and ablated lesion, was then transported en bloc to the pathology department for immediate processing. Specimens were inspected and measured by the pathologist. Scaled digital photographs were taken and were later correlated with the gross pathologic measurements to ensure the accuracy of the ablation zone size. Representative regions of interest, which included grossly coagulated and viable tumor, coagulated and viable liver parenchyma, and equivocal areas within the transition zone were then frozen for further sectioning. These sections were stained separately with the standard H and E stain and vital histochemical nicotinamide adenine dinucleotide (NADH) stain.

In regions where H and E staining proved equivocal, staining with NADH stain, which has an unambiguous binary staining characteristic of positive staining indicating tissue viability and nonstaining indicating cellular death, was used to prove or disprove tissue viability [7]. In all cases, the primary diagnosis of liver malignancy was confirmed by standard histologic criteria. Tumor histology included six CRC metastases and four HCCs. Resection margins were also scrutinized for tumor according to standard clinical protocol.

Volumetric Calculations
The approximate volumes of tumor and ablation coagulation zone were calculated assuming an ellipsoid geometry using the following:

Formula
where V is volume, and x, y, and z represent the diameters (in centimeters) of the three orthogonal axes.


Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Tumor and Ablation Zone Characteristics
The mean maximal tumor diameter was 4.4 cm (range, 2.0-5.7 cm), and the average tumor volume was 33.0 cm3 (2.3-76.3 cm3). The mean maximal ablation diameter was 5.5 cm (5.0-6.5 cm), and the average ablation zone volume, assuming ellipsoid geometry, was 50.8 cm3 (30.3-65.5 cm3). The measurements of the ablation zones in the x, y, and z orthogonal planes are summarized in Table 1. In all ablations, the individual lesion components had completely fused to create one large continuous ablated volume that encompassed the grossly visible tumor mass in its entirety. Nevertheless, on closer inspection, some cross sections, those that were perpendicular to the plane of the antenna shaft, revealed that the ablated lesion shapes were not strictly circular but, rather, took on a slightly triangular contour. This "deformation" was considered minimal because no grossly apparent clefts appeared along the coagulated border.

Histopathologic and Tumor Histochemical Characteristics
On gross inspection of the ablated zone, a central pale zone of coagulation surrounded by a red hyperemic zone was visualized (Fig. 4). The three microwave antenna tracts were visualized, via careful cross sectioning, to be in the center of each ablation volume, which in turn completely surrounded the liver tumor.


Figure 6
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  		Fig. 4 —Scaled digital photograph taken of resected gross specimen from a 67-year-old man with colorectal carcinoma metastases (patient 6 in Table 1) shows ablation zone extending to hepatic vein (large arrow). Three microwave antenna sites (small arrows) are seen in center of ablation zone. Note central pale zone of coagulation surrounded by red hyperemic zone.

 
Microscopically, on initial H and E staining, hepatocytes within the central coagulated zone had an amorphous cytoplasm, with loss of all cellular structure and no discernible cell membranes. Although some cells did retain the appearance of cellular nuclei, on further examination with the vital histochemical NADH stain for the mitochondrial enzyme NADH diaphorase [7], no viable tissue was seen.

Moving further from the primary (central) coagulation zone into the surrounding zone of hyperemia, some H and E-stained areas displayed only a subtle loss of nuclear chromatin detail with minimal cell membrane destruction. However, using the unambiguous staining characteristic of the histochemical NADH stain [7], we were able to confidently discern areas of cellular viability versus areas of cellular death at the margin—all within normal liver. At the 5-mm transition zone between grossly coagulated and clearly viable tissue, NADH staining consistently revealed uniform cellular death with a sharp border demarcating viable from ablated regions (Figs. 5A, 5B, 5C, and 5D).


Figure 7
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  		Fig. 5A —Photomicrographs of colorectal carcinoma (CRC) metastases to liver and of normal liver. Photomicrographs of same sections of liver from 54-year-old man (patient 2 in Table 1) with CRC metastases stained with H and E stain (A) and vital histochemical nicotinamide adenine dinucleotide (NADH) stain (B) show complete microwave thermocoagulation of all areas (magnification, x100). Note this effect is more clearly seen on NADH-stained slide (B).

 

Figure 8
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  		Fig. 5B —Photomicrographs of colorectal carcinoma (CRC) metastases to liver and of normal liver. Photomicrographs of same sections of liver from 54-year-old man (patient 2 in Table 1) with CRC metastases stained with H and E stain (A) and vital histochemical nicotinamide adenine dinucleotide (NADH) stain (B) show complete microwave thermocoagulation of all areas (magnification, x100). Note this effect is more clearly seen on NADH-stained slide (B).

 

Figure 9
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  		Fig. 5C —Photomicrographs of colorectal carcinoma (CRC) metastases to liver and of normal liver. For comparison with A and B, photomicrographs of sections from same patient of normal liver parenchyma obtained after microwave ablation and stained with H and E (C) and NADH (D) stains show complete thermocoagulation on left half of slide but viable tissue on right (magnification, x100). Note dark blue area (viable cells) on right is more evident on NADH-stained slide (D).

 

Figure 10
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  		Fig. 5D —Photomicrographs of colorectal carcinoma (CRC) metastases to liver and of normal liver. For comparison with A and B, photomicrographs of sections from same patient of normal liver parenchyma obtained after microwave ablation and stained with H and E (C) and NADH (D) stains show complete thermocoagulation on left half of slide but viable tissue on right (magnification, x100). Note dark blue area (viable cells) on right is more evident on NADH-stained slide (D).

 

Large blood vessels (> 3 mm in diameter) in the resection specimens did not create the typical ablation zone distortion that might be expected with other thermoablative techniques due to the minimal heat sink effect observed with microwave ablation (Fig. 6). A marked thermallike effect was observed with maximal intensity closest to the antenna site.


Figure 11
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  		Fig. 6 —Digital photograph of resected gross specimen from a 67-year-old man with colorectal carcinoma metastases (patient 8 in Table 1) stained with nicotinamide adenine dinucleotide (NADH) shows area of marked thermocoagulation surrounding 4-mm hepatic vein.

 
Of particular interest, in one patient who had undergone oxaliplatin chemoembolization 1 year before microwave ablation and subsequent liver resection, the ablated region encompassing the CRC metastasis microscopically showed severe architectural and cellular distortion of the fibrosed and hyalinized adenocarcinoma, more severe than any of the previous cases, with resultant foci of barely recognizable nonviable liver and tumor tissue. Grossly, the extent of the microwave ablation effect was also larger and more confluent than previous CRC metastasis ablations in our series.

Complications
No direct procedural complications secondary to microwave ablation were noted. The following complications were deemed to be temporally and causatively related to the hepatic resection and were encountered in four patients: non-Q wave myocardial infarction (reported surgical morbidity rate [8], 2%; range, 1-4%), renal failure and staphylococcal bacteremia (3%; range, 1-37%), hepatic failure salvaged by orthotopic liver transplantation (4%; range, 0.5-28%), and perihepatic abscess (4%; range, 1-28%) complicated by lower extremity ischemia that resulted in eventual death (5%).


Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Although resection of HCC and hepatic CRC metastases has been shown to increase both the 5-year overall and the disease-free survival [9-11], many patients may have tumors that are surgically unresectable because of either unfavorable tumor anatomy or poor patient hepatic reserve. Radiofrequency ablation is currently the dominant thermal ablation technique in use worldwide. Other potential thermoablative energy sources include laser, high-intensity focused ultrasound, and microwave ablation. There are many different strategies for applying these thermal energies including, but not limited to, single straight electrodes, multiple expandable electrodes, pulsed energy delivery systems, and internally cooled systems. Based on this wide variety of choices, a substantial debate has emerged as to which of the techniques and which of the electrode or delivery modifications are most appropriate for specific clinical scenarios.

In addition, adequate treatment outcomes and clinical successes are often determined by various biophysical limitations, such as the ideal tumor biology (tumor histology, presentation, and growth rate), blood flow characteristics (both intratumoral and surrounding the tumor), and tissue conductance. Factors such as the local tissue composition may alter the extent of coagulation because heat conducts differently throughout different tissue types at various rates. Local dielectric properties can often times prove advantageous when it results in improved (increased) heat retention during the ablations, such as in the treatment of HCC surrounded by cirrhotic tissue [12], lung tumors with surrounding aerated lung [13], and vertebral body lesions surrounded by bone cortex [14].

Commonly reported disadvantages in the current thermoablation systems include difficulty in treating large tumors—that is, those exceeding 3 cm in diameter [15]; the potential for incomplete radiofrequency tumor ablation near blood vessels because of the heat sink effect of local blood flow [16]; difficulty in obtaining sonographic images of radiofrequency lesions [17]; and evidence of surviving tumor cells, even within radiofrequency lesions [18]. The treatment of large tumors can be time consuming to adequately ensure total overlapping coverage of the ablation zones. Even with meticulous technique, tumor recurrence can be frequent [15]. Thus, the use of multiple electrodes to achieve larger coagulation volumes than possible with a single electrode has been proposed.

In this regard, however, a significant difference in the physics of microwave ablation and radiofrequency ablation should be noted. Radiofrequency ablation involves the flow of current, in the frequency of radiowaves, within the body tissues using conductive electrodes. Essentially, the alternating radiofrequency current causes surrounding ions in adjacent tissue to oscillate and collide in proportion to the intensity of the radiofrequency current. This generates enough heat, greater than the cytotoxic threshold, thus leading to cellular death via thermocoagulation necrosis.

Alternatively, microwave ablation generates an electromagnetic wave around insulated, electrically independent antennas. This electromagnetic wave causes the agitation of polar water molecules within surrounding tissue. This vigorous movement of water molecules then raises the temperature within the adjacent tissue causing frictional heating, thus inducing cellular death via coagulation necrosis. Therefore, microwaves (at least theoretically) should be more amenable than radiowaves to synchronous ablations using multiple applicators to achieve larger tumor coagulation volumes in shorter periods of time. Percutaneous radiofrequency ablation is currently considered the first-line treatment for small (< 3 cm) HCC in nonsurgical candidates [19, 20].

Microwave ablation offers many of the benefits of radiofrequency ablation but has several theoretic advantages that may result in improved performance near blood vessels. During radiofrequency ablation, the zone of active tissue heating is limited to a few millimeters surrounding the active electrode, with the remainder of the ablation zone being heated via thermal conduction [21]. Owing to the much broader field of power density of the electromagnetic microwave (up to 2 cm surrounding the antenna), microwave ablation results in a much larger zone of active heating than radiofrequency ablation [22]. This has the potential to allow a more uniform tumor kill in the ablation zone, both within the targeted zone and the blood vessels next to the targeted zone. Radiofrequency ablation is also limited by the increase in impedance with tissue boiling and charring [23] because water vapor and char act as electric insulators. Due to the electromagnetic nature of the microwave, ablations performed do not seem to be subject to this limitation, thus allowing the intratumoral temperature to be driven considerably higher, resulting in a larger ablation zone within a shorter ablation time period.

The use of microwave ablation, originally referred to as "microwave coagulation therapy," has been most prevalent to date in Asia, where a number of reported studies have shown it to be effective in the local control of both HCC [24, 25] and metastatic CRC [26]. The Asian system uses a smaller microwave applicator at 2.4 GHz that creates small ablation sizes, thereby making it difficult to treat large lesions. The new 915-MHz microwave system that we used is more tuned to the dielectric properties of human tumor tissue. Given this and the size of current microwave applicators, large ablation volumes can now be achieved in fewer applications.

The initial experiments by other investigators using this new microwave ablation system with a porcine liver model have been encouraging [4]. Ablation volumes obtained with simultaneous multiple straight probe ablations were significantly larger than the same number of ablations made sequentially. In addition, these larger volumes were obtained in the time required for a single ablation cycle, by virtue of the simultaneous powering on of all microwave antennas. In this preliminary clinical setting of this device in the treatment of human liver tumors, our results appear comparable. Using a triple straight microwave antenna configuration, we created large ablation volumes of approximately 50.8 cm3 in 10 minutes.

In addition, it is easier to target and appropriately place multiple microwave antennas within a lesion compared with trying to place one radiofrequency electrode in an untreated area by moving the electrode. Subsequent placing of an additional microwave antenna 2 cm from one that is already in place is much easier and more accurate than performing the task without an antenna in place. Besides the synergistic use of multiple microwave antennas in the treatment of solitary lesions, the ability to drive multiple antennas simultaneously may be useful in the treatment of multiple tumors. With radiofrequency ablation usually requiring between 12 and 25 minutes per lesion, the total procedure time can be quite lengthy, especially when attempting to treat multiple tumors. Significant time savings could be achieved through microwave ablations with multiple antennas given the better convection profile of microwave ablation when compared with radiofrequency ablation.

One potential disadvantage of this triple straight antenna configuration is the fact that ablations tended to result in a nonspherical volume, which may have been expected given the triangular arrangement of the three microwave antennas. Wright et al. [4] reported in a porcine study that antenna separation of < 1.7 cm yielded significantly rounder, more confluent-looking lesions. However, with antenna separation of > 1.7 cm, the overall ablated lesion became less spherical. We observed this same slight loss of border convexity in some ablation specimen cross sections, but in all cases, the zones of coagulation had adequately fused without spared tissue between the antennas.

Hepatic ablation is currently being used to treat and increase the number of patients amenable to curative or palliative treatment of liver cancers [27]. All current systems have unique advantages and disadvantages. Cryoablation has been widely studied intraoperatively, with higher complication rates reported when compared with radiofrequency ablation [28]. Newer percutaneous cryotherapy systems may allow cryoablation to be used in more patients with liver tumors. Theoretic problems with percutaneous cryoablation include bleeding requiring additional maneuvers such as tract coagulation with fibrin glue. Radiofrequency ablation is time consuming; is limited to single lesions; and seems to have higher recurrence rates, especially near blood vessels larger than 3 mm [16]. This new microwave ablation system currently has several theoretic advantages over radiofrequency ablation, including an improved convection profile with consistently higher intratumoral temperatures, larger tumor ablation volumes and faster ablation times, and the ability to simultaneously use multiple antennas.

In conclusion, we believe this study has shown the feasibility of using simultaneous multiple microwave antennas in the treatment of liver tumors intraoperatively. Additional percutaneous studies are currently under way to investigate the safety and efficacy in treating patients who are not candidates for hepatic resection.


References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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T. M. Pawlik, R. D. Schulick, and M. A. Choti
Expanding Criteria for Resectability of Colorectal Liver Metastases
Oncologist, January 1, 2008; 13(1): 51 - 64.
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