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Inter ventional Radiolog y • Original Research
Simon et al.
Intraoperative Triple
Antenna Hepatic
Microwave Ablation
A
C E N T U
R Y
MEDICAL
O F
IMAGING
Caroline J. Simon1
Damian E. Dupuy1
David A. Iannitti2
David S. K. Lu3
Nam C. Yu3
Bassam I. Aswad4
Ronald W. Busuttil5
Charles Lassman6
Simon CJ, Dupuy DE, Iannitti DA, et al.
Keywords: liver metastases, microwave ablation,
radiofrequency ablation, radiologic–pathologic correlation
DOI:10.2214/AJR.05.0804
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.
1Department
of Diagnostic Imaging, Brown Medical
School, Rhode Island Hospital, 593 Eddy St., Providence, RI
02903. Address correspondence to D. E. Dupuy
(ddupuy@lifespan.org).
2Department
of Surgery, Brown Medical School, Rhode
Island Hospital, Providence, RI.
3Department of Diagnostic Imaging, David Geffen School of
Medicine at UCLA, Los Angeles, CA.
4Department
of Pathology, Brown Medical School, Rhode
Island Hospital, Providence, RI.
5Department of Surgery, David Geffen School of Medicine
at UCLA, Los Angeles, CA.
6Department
of Pathology, David Geffen School of
Medicine at UCLA, Los Angeles, CA.
WEB
This is a Web exclusive article.
AJR 2006; 187:W333–W340
0361–803X/06/1874–W333
© American Roentgen Ray Society
AJR:187, October 2006
Intraoperative Triple Antenna
Hepatic Microwave Ablation
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.
epatic 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 inter-
H
val [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
W333
Simon et al.
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
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.
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).
Microwave Ablation Treat and Resect Protocol
All microwave ablations were performed intraoperatively 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 ab-
TABLE 1: Patient and Tumor Characteristics with Ablation Zone Sizes
Patient
Ablation Size (cm)
x
y
z
Ablation
Volume (cm3)
2.5
6.5
2.5
4.0
34.0
CRC
2.0
5.0
5.0
4.5
58.9
CRC
2.0
5.0
5.0
4.5
58.9
F
CRC
1.5
4.0
4.5
5.6
52.8
M
HCC
1.5
5.0
3.0
6.3
49.5
67
M
CRC
1.5
3.0
3.5
5.5
30.3
7
77
M
HCC
2.0
4.5
4.5
5.0
53.0
8
67
M
CRC
2.0
5.0
5.0
5.0
65.5
9
79
F
HCC
2.0
3.8
4.6
5.0
45.8
10
53
F
HCC
2.0
6.0
5.5
3.4
58.8
Tumor
Antenna
Histology Spacing (cm)
No.
Age (y)
Sex
1
48
F
CRC
2
54
M
3
70
F
4
67
5
57
6
Note—CRC = colorectal carcinoma metastases, HCC = hepatocellular carcinoma.
W334
lation. 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 (Fig. 3).
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.
AJR:187, October 2006
Intraoperative Triple Antenna Hepatic Microwave Ablation
Volumetric Calculations
The approximate volumes of tumor and ablation
coagulation zone were calculated assuming an ellipsoid geometry using the following:
V = 1/6 × π × x × y × z,
where V is volume, and x, y, and z represent the diameters (in centimeters) of the three orthogonal axes.
Results
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 cir-
Fig. 1—Photograph shows
single straight microwave
antenna (VivaTip Surgical,
Vivant Medical) with 3.6cm active tip.
47
cular 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.
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 (Fig. 5).
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.
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%).
Fig. 2—Digital
photograph of 48-yearold 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.
Discussion
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
AJR:187, October 2006
W335
Simon et al.
A
B
Fig. 3—48-year-old woman with colorectal carcinoma metastases (patient 1 in
Table 1).
A–C, Sequential sonograms (taken 1–2 minutes apart) show development of
exuberant transient hyperechogenic response in surrounding liver parenchyma to
microwave ablation.
C
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AJR:187, October 2006
Intraoperative Triple Antenna Hepatic Microwave Ablation
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
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.
AJR:187, October 2006
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 ab-
W337
Simon et al.
lations were significantly larger than the same
number of ablations made sequentially. In ad-
dition, 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
A
B
C
D
Fig. 5—Photomicrographs of colorectal carcinoma (CRC) metastases to liver and of normal liver.
A and B, 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, ×100). Note this effect is more clearly seen on
NADH-stained slide (B).
C and D, 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, ×100). Note dark blue area (viable cells) on
right is more evident on NADH-stained slide (D).
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AJR:187, October 2006
Intraoperative Triple Antenna Hepatic Microwave Ablation
tently 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.
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.
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ablation volumes of approximately 50.8 cm3
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AJR:187, October 2006
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