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Perspective |
1
Department of Radiology, University of California, Davis Medical Center, 4860
Y St., Ste. 3100, Sacramento, CA 95817.
2
Department of Radiology, University of Texas Health Science Center at San
Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78229-3900.
Received February 22, 2000;
accepted after revision June 5, 2000.
Address correspondence to J. P. McGahan.
Introduction
 Top Introduction BackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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A number of alternative therapies have been used for the treatment of malignant hepatic tumors. These include chemoembolization, ethanol injection therapy, and thermal ablation techniques. Chemoembolization has been studied extensively and is often reserved for patients with unresectable hepatic tumors [8, 9]. Ethanol injection therapy has gained fair international acceptance as a safe, inexpensive, and effective therapy for small HCC tumors [10, 11]. However, it has failed to generate much enthusiasm in the United States. This lack of enthusiasm is based in part on the need to perform multiple consecutive therapeutic sessions to completely kill even the smallest HCC tumor and the fact that the technique is typically performed under sonographic guidance [11]. Furthermore, ethanol injection therapy has been shown to be ineffective for the treatment of colorectal metastases [12].
Thermal ablation techniques for the treatment of malignant hepatic tumors include both freezing (cryoablation) and heating (radiofrequency, microwave, laser, and high-intensity focused sonography) techniques. Of these techniques, cryoablation has been the most extensively investigated [13, 14]. The two advantages of cryoablation over surgical resection are that it can be used to treat liver tumors that, by number or location, are not surgically resectable, and that it is associated with diminished morbidity and mortality relative to resection. The overall prognosis for patients undergoing cryoablation is reported to be the same as for hepatic resection. However, the limitations of cryoablation are similar to the limitations of hepatic resection—namely, it is invasive, with a laparotomy being performed in most cases [14].
During the last 10 years, considerable interest has developed in the thermal ablation techniques that produce heat. Methods that are being investigated include microwave, laser, high-intensity focused ultrasound, and radiofrequency ablation. Most of the research on microwave ablation has been performed in Japan, with minimal experience or knowledge of the technique outside that country [15, 16]. Laser ablation has been tested most rigorously outside the United States [17,18,19]. One group of German researchers, Vogl et al. [19], claim that the technique is highly effective for the treatment of both HCC and colorectal metastases. However, one of the primary investigators of laser ablation in England has essentially abandoned the technique in favor of radiofrequency ablation [20]. High-intensity focused ultrasound has been shown to be successful in ablating hepatic tumors in animal models but has not been used to treat liver tumors in humans [21]. Overall, the interest and enthusiasm for radiofrequency thermal ablation has far exceeded that for either microwave or laser ablation. This article will review the current status of radiofrequency ablation in the treatment of liver neoplasms
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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In the early 1990s, two independent groups of investigators using modified radiofrequency equipment studied the percutaneous creation of focal thermal injuries deep in the liver [31, 32]. In their studies they used equipment similar to that of the Bovie knife; that is, an alternating electric current generator operated in the radiofrequency range, a grounding pad placed on the tissue, and an insulated needle as a monopolar electrode. The original needle design was simple and used standard stock needles insulated to the distal tip (Fig. 1A,1B). The studies consisted of placing needle electrodes deep in the liver and creating focal thermal injuries around the noninsulated tip of the needles. Gross and histologic examination of the ablated livers showed that the process produced a well-defined concentric region of coagulative necrosis around the exposed needle tip. This was similar to coagulative necrosis as described in prior experimentation [33]. However, the size of the thermal injuries was small; the radius of the coagulated tissue surrounding the exposed needle tip was approximately 1 cm (Fig. 2A,2B). Superficial charring around the needle tips similar to that produced by the Bovie knife limited the size of the thermal injury that could be created in the liver. Nonetheless, both investigators proposed that radiofrequency ablation might be an effective technique for destroying small malignant liver tumors [31, 32].
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Subsequent research has shown that effective tissue coagulation requires local temperatures in excess of 50°C [34]. Furthermore, several factors, including a slow increase in generator power, prolonged radiofrequency application, and an increase in the exposed surface area of radiofrequency needle electrodes, have been shown to increase the volume of coagulated tissue [34,35,36].
Modern radiofrequency ablation equipment can create thermal lesions of sufficient size (3-4.5 cm) to be clinically relevant. In the United States, three primary companies (RITA Medical Systems, Mountain View, CA; Radiotherapeutics, Mountain View, CA; and Radionics, Burlington, MA) market radiofrequency devices for tissue ablation. Each of the companies received approval of their devices from the Food and Drug Administration under a 510K-like device exemption. The radiofrequency tissue ablation devices were deemed similar enough to the Bovie knife in design and application that a full Food and Drug Administration application was unnecessary. Each company was allowed to market its device for generic tissue ablation; however, none could market its device specifically for the ablation of hepatic tumors. However, just recently the Food and Drug Administration has approved the use of these devices for the treatment of liver tumors that are surgically unresectable.
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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One of the manufacturers markets a system with two retractable needle electrodes (Model 70 and Model 90 Starburst XL Needles; RITA Medical Systems). The needle electrodes consist of a 14- or 15-gauge insulated outer needle that houses seven or nine (respectively) retractable curved electrodes of various lengths. When the electrodes are extended, the devices assume the approximate configuration of a Christmas tree, with the length and diameter of the electrode clusters measuring 3 or 5 cm, respectively (Fig. 3A). Four of the electrodes are hollow and contain thermocouples in their tips that are used to measure the temperature of the adjacent tissue. The alternating electric current generator comes in either a 50- or 150-W model; both are operated at 460 kHz. To perform a typical ablation, one or two grounding pads are placed on the patient's back or thigh. The tip of the needle (with retracted electrodes) is advanced to the desired location, and the electrodes are deployed to approximately two thirds their length. The generator is turned on and run by an automated program. The program starts the generator at approximately 25 W and then gradually increases the wattage to peak power in 30-120 sec. The program monitors the temperature at the tips of the electrodes and maintains peak power until the temperature exceeds the preselected target temperature (typically between 95° and 105°C). The operator watches the temperature display, and after the target temperature is achieved, advances the curved electrodes slowly to full deployment while maintaining the target temperature. When the electrodes are fully deployed, the program maintains the target temperature by regulating the wattage. As the tissue begins to desiccate, the amount of power needed to maintain the target temperature decreases. The company recommends that the target temperature be maintained for 8-12 min for the smaller electrode and 25 min for the larger electrode. After the ablation cycle is completed, a temperature reading from the extended electrodes in excess of 50°C at 1 min is reported to indicate a satisfactory ablation [34].
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Another radiofrequency ablation device (LeVeen Needle Electrode; Radiotherapeutics) has retractable curved electrodes and an insulated 14-gauge outer needle that houses 10 solid retractable curved electrodes that, when deployed, assume the configuration of an umbrella [37] (Fig. 3B). The electrodes are manufactured in different lengths (2- to 3.5-cm umbrella diameter), with most users choosing the 3.5-cm device. The alternating electric current generator is 100 W operated at 480 kHz. Two ground pads are used with the device; both are placed on the patient's thighs. In application, the tip of the radiofrequency needle is advanced to the target tissue and the curved electrodes are deployed to full extension. The generator is switched on and immediately set to 30 W. Every 60 sec the wattage is increased by 10 until peak power (90 W) is attained. The device is maintained at peak power for 15 min or until it "impedes out" (i.e., a rapid rise in impedance stops current flow and the ablation). If the device impedes out, it is turned off for 30 sec and then restarted at 70% of the maximum power attained at the time the generator impeded out. The application continues until the generator once again impedes out or for 15 min. If the device did not impede out during the first cycle, it is switched off for 30 sec and then restarted at maximum power and run until it impedes out or 15 min has elapsed. The Radiotherapeutics ablation algorithm is based on tissue impedance rather than tissue temperature. The power settings are increased slowly to minimize early tissue desiccation and charring. The impedance of the tissue increases as the tissue desiccates. It is believed that an ablation is successful if the device impedes out.
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A third manufacturer has taken an entirely different approach to needle electrode design. They use an insulated hollow 17-gauge needle with a exposed needle tip of variable length (2-3 cm) (Cool-Tip radiofrequency electrode; Radionics). The tip of the needle is closed and contains a thermocouple for recording the temperature of the adjacent tissue. The shaft of the needle has two internal channels to allow the needle to be perfused with chilled water. Two groups of investigators have shown that the cooled needle produces a larger ablation than does a similar non-perfused needle [38, 39]. Conceptually, the cooling is believed to prevent desiccation and charring around the needle tip; thus, ionic agitation, frictional heat, and the size of the thermal injury produced are maximized. In an attempt to further increase the size of the ablation, the company placed three of the cooled needles in a parallel triangular cluster with a common hub (Fig. 3C). Goldberg et al. [40] tested this device and found that it produces a significantly larger ablation than does a single cooled needle.
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The generator provided with the cooled-tip radiofrequency needles is the
most powerful of the three commercially available generators. It has a peak
power output of 200 W and is operated at 480 kHz. In clinical application,
four grounding pads are placed on the patient's thighs. The tip of the single
or cluster electrode is advanced to the desired location in the tissue to be
treated. To maintain the correct spacing and triangular configuration of the
cluster needle, a guidance thimble is used
(Fig. 4). The single or cluster
electrode needles are connected both to the generator and to a perfusion pump.
The pump is switched on and sterile chilled water is circulated through the
needle. To begin the ablation, an automated program gradually increases the
power for 1 min to a peak of 200 W and maintains the power at that level until
the impedance rises 20 
over the starting level. The power is then
reduced automatically to 10 W for 15 sec and then returned to maximal power
until the impedance increases again. If the power cannot be maintained for at
least 10 sec without a rise in the impedance, the power is reduced for
subsequent cycles to minimize elevations in impedance. Successive cycles are
continued for a total ablation time of 12 min. Successful ablations usually
increase the temperature of the ablated tissue to between 60° and
80°C.
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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Preoperative Evaluation
The preoperative evaluation begins with a review of the pertinent imaging
studies. Goodquality abdominal CT or MR imaging is the fundamental imaging
examination on which the candidacy of a patient for radiofrequency ablation is
based. These preoperative imaging studies are used to determine the number and
size of tumors and their relationship to surrounding structures such as blood
vessels, bile ducts, gallbladder, diaphragm, and bowel. Patients are
considered potential candidates if they have fewer than five tumors, each less
than 5 cm in diameter, and no evidence of extrahepatic tumor
[6,
40,41,42].
In practice, patients with more than two tumors approaching 5 cm are poor
candidates because of the sheer bulk of their tumor burden and the difficulty
in completely ablating tumors of such size. By far the most common liver
tumors that have been treated with radiofrequency ablation are HCC tumors and
colon metastases. In addition, we have treated metastatic tumors from the
pancreas, breast, stomach, and neck, as well as metastatic neuroendocrine
tumors. In fact, any type of tumor isolated to the liver that meets our
criteria can be treated by radiofrequency ablation. However, patients with
potentially resectable tumors should be told that hepatic resection is the
standard of care, and then referred for surgical evaluation.
Tumors close to the vital structures require careful consideration. We have found that ablation of tumors adjacent to the diaphragm, liver capsule, gallbladder, or main portal vessels will cause considerably more pain during and after the procedure than will ablation of tumors embedded in the hepatic parenchyma. Ablation of tumors adjacent to the diaphragm will cause transient right shoulder pain; however, if the diaphragm is directly ablated, as occurred in one of our patients, the pain can be severe and last for several months. The ablation of a tumor touching the wall of the gallbladder can lead to the development of cholecystitis, with symptoms lasting 2-3 weeks. Tumors adjacent to large vessels may be difficult to completely ablate because the blood flow in the vessel cools the tissue and may prevent adequate heating. Careful consideration needs to be given to the treatment of tumors lying in the bifurcation of the right and left portal veins or adjacent to either main portal trunk. Aside from the increased pain for the patient and diminished ability to effectively heat tumors in these locations, a very real risk exists of damaging the main right or left bile ducts. If the ducts are injured, the likely sequela is biliary obstruction. Finally, the treatment of subcapsular tumors abutting other abdominal viscera poses the risk of damage to those organs. Of greatest concern in this regard is the possibility of inducing thermal necrosis in an adjacent loop of bowel [43, 44].
If a patient is a good candidate for thermal ablation on the basis of his
or her baseline abdominal CT or MR imaging, then a series of other tests is
indicated before actual treatment. All patients should have histologic
confirmation of a hepatic malignancy. CT of the chest should be performed to
rule out the possibility of pulmonary metastases. A serum alkaline phosphatase
level should be obtained; if the level is elevated without other just cause,
or if the patient has new unexplained bone pain, technetium bone scanning
should be performed to exclude the possibility of bone metastases. If the
ablation procedure is to be performed using sonographic guidance, targeted
hepatic sonography should be performed to determine if the lesions can be seen
on sonography and to determine if a safe and adequate approach exists.
Hematologic evaluation is necessary because the ablation needles are fairly
large (14- to 17- gauge), and multiple percutaneous transhepatic needle
punctures may be necessary to complete an ablation. Hematology tests should
include a complete blood count, hemoglobin, hematocrit, prothrombin time,
partial prothrombin time, and a platelet count. Coagulopathies should be
corrected before an ablation session. A routine serum chemistry panel should
be obtained to check electrolytes and liver function. A baseline serum
-fetoprotein and a carcinoembryonic antigen level should be obtained in
patients with HCC and colorectal metastases, respectively. On the day before
an ablation session, and ECG and blood type and match should be obtained in
preparation for possible emergent surgery that may be necessary to treat a
significant complication caused by the ablation. Contraindications to
performing radiofrequency thermal ablation of hepatic tumors include excessive
intrahepatic tumor burden, untreatable extrahepatic tumor, Child's class C
cirrhosis, active infection, and inability to execute a proper consent.
Choice of Approach: Percutaneous, Laparoscopy, or Laparotomy
At our institutions, whenever possible radiofrequency ablation is performed
percutaneously. Percutaneous treatment has several advantages over other
approaches. The percutaneous approach is the least invasive, produces minimal
morbidity, can be performed on an outpatient basis, requires only conscious
sedation, is relatively inexpensive, and can be repeated as necessary to treat
recurrent tumor. However, advocates of laparoscopic thermal ablation of
hepatic tumors claim that the laparoscopic approach provides some distinct
advantages over the percutaneous approach
[45]. With the laparoscopic
technique, the entire liver can be imaged with a high-frequency transducer
placed directly on the surface of the liver. This technique allows the
visualization (and treatment) of small tumors that cannot be detected using
any other imaging technique (Fig.
5A,5B).
Furthermore, with laparoscopy the extent of a tumor can be more accurately
staged. The identification of previously undetected surface lesions or
peritoneal implants may lead to the appropriate cancellation of the planned
radiofrequency ablation [46].
This is important if the goal of the procedure is potential cure. However,
Siperstein et al. [45] have
also used laparoscopic radiofrequency for symptomatic relief of hormonally
active liver metastasis. Additionally, advocates of a laparoscopic approach
argue that they can perform a Pringle maneuver (temporary occlusion of the
hepatic artery and portal vein) and thus enhance the size of a thermal
ablation. The disadvantages of a laparoscopic approach include the added
invasiveness of the procedure, with the associated complications and added
costs, and the technical difficulties of the procedure. In particular, the
placement of the needle electrode can be problematic. Unlike the percutaneous
technique in which the sonographic probe and radiofrequency needle can be
moved to any position over the right upper quadrant to achieve the best angle
of approach to treat a tumor, the laparoscopic technique is hampered by
limited access through the existing laparoscopic ports. Furthermore, no needle
guides are currently available that can be attached to the laparoscopic
sonographic transducers, and the radiofrequency needles cannot be placed
parallel to the transducers. Most commonly, the needles are placed either
perpendicular or oblique to the sonographic transducers. The manipulation of
the needle from these angles is technically challenging and is not easily
mastered.
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Other investigators have published their experiences with radiofrequency ablation performed via open surgical treatment [42]. Disadvantages of this technique include the associated morbidity and mortality of an open procedure and general anesthetic, the added expense of the procedure and associated recovery time, and the fact that the technique is typically a one-shot therapy. Some of the advantages of the technique are the same as for the laparoscopic approach—namely, the ability to scan the whole liver with high-frequency transducers and to accurately stage the extent of the tumor [47] (Fig. 5A,5B). Additionally, the open approach allows a great deal of freedom in placing the sonographic transducer and radiofrequency needle. The radiofrequency needle can be placed through a needle guide that is attached to the transducer, or it can be placed using a freehand technique. Difficult lesions adjacent to the diaphragm, bowel, or gallbladder may be treated easily with the open technique. These organs can be removed or isolated from the mobilized liver to prevent damage during the ablation of a tumor (Fig. 6). Finally, the blood supply to the liver may be temporarily stopped during radiofrequency ablation. A Pringle maneuver, which causes temporary occlusion of the portal vein and hepatic artery, decreases blood supply to both the targeted tumor and the adjacent hepatic parenchyma. The result is a larger thermal injury than is possible with normal blood flow [42].
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Anesthesia and Medications
General anesthesia is required for laparoscopy or open surgical treatment.
However, conscious sedation is usually sufficient for a percutaneous approach.
At our institutions, we use the services of the anesthesiology department for
percutaneous radiofrequency ablation. On the morning of the procedure, an
anesthesiologist or nurse-anesthetist evaluates the patient for suitability
for anesthesia. The medical history is reviewed, the laboratory test results
are checked, and the ECG is interpreted. If deep conscious sedation is not
contraindicated, the patient is prepared for the procedure. A peripheral IV
line is started, and the patient is monitored to track blood pressure, pulse,
respiratory rate, and peripheral oxygenation. The site of the planned
percutaneous puncture with the radiofrequency electrode is anesthetized with
1% lidocaine hydrochloride (Xylocaine; AstraZeneca, Wilmington, DE). The
anesthesiologist or nurse-anesthetist administers an IV sedative. This can be
a combination of the traditional drugs fentanyl (fentanyl citrate injection;
Elkins-Sinn, Cherry Hill, NJ or Baxter Healthcare, Deerfield, IL) and
midazolam hydrochloride (Versed; Roche Laboratories, Nutley, NJ) that are used
for many percutaneous intervention procedures, or, as we prefer, the more
potent and short-acting agents propofol (Diprivan; Astra-Zeneca) or
remifentanil hydrochloride (Ultiva; Glaxo Wellcome, Research Triangle Park,
NC) [48]. These newer agents
are administered by a constant drip infusion. The major advantages of these
agents are the deep level of anesthesia that can be obtained and their short
duration of action. If the cooperation of a patient is needed to achieve
satisfactory placement of the needle electrode, the patient is easily aroused
within minutes of stopping the infusion of the agent. Likewise, if a patient
has respiratory suppression due to oversedation, he or she is quickly
recovered by stopping the infusion and ventilating the patient using a bouche
bag for a few minutes.
At the end of a radiofrequency ablation session, the patient can experience severe nausea and pain with the decrease of the sedative. Because of the frequency of these two side effects, we established a routine protocol to treat these problems. Immediately after the conclusion of the procedure and before transporting the patient to the recovery area, we administer both an antiemetic and morphine IV. After the patient is transferred to the recovery area, combined oral hydrocodone bitartrate and acetaminophen tablets (Vicodin; Knoll Laboratories, Mount Olive, NJ), are given to control subacute pain. This medication regime is usually sufficient to keep the patient comfortable for 3-4 hr, at which time the side effects of the ablation have usually diminished to a tolerable level. Fewer than 50% of patients require additional analgesics during the immediate recovery period, and even fewer require analgesics after discharge. If pain persists, the patient is typically given a 3-day prescription for combined oral hydrocodone bitartrate and acetaminophen tablets (Vicodin).
Occasionally, patients may be unable to tolerate percutaneous radiofrequency ablation with just conscious sedation. This may be true for patients with cancer with chronic pain who have been taking routine analgesics, patients with a history of alcohol or drug abuse, or patients with a low tolerance for pain. General anesthesia may be indicated for these patients. Likewise, general anesthesia may be preferred if an ablation is going to be extensive and the procedure is expected to last 3 hr or longer.
Although there has been no trial to validate the use of prophylactic antibiotics, such use has become routine at some institutions. One of us routinely administers IV cephalosporin just before treatment and continues with oral cephalosporin for 5 days after treatment.
Needle Placement and Treatment Strategy
Radiofrequency needles can be placed under sonographic, CT, or MR guidance
using a percutaneous approach. The needles are usually well revealed by each
technique (Fig.
7A,7B).
However, without question sonography is the most common method used to guide
percutaneous radiofrequency tumor ablation
[49,50,51,52,53,54,55,56,57,58,59].
Its advantages over CT and MR are its realtime capabilities, vascular
visualization, availability, speed, and low cost.
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The primary disadvantage of sonography is a limited ability to assess the effectiveness of an ablation. Although the ablation process produces a dense echogenic response, the size of the echogenic response provides only a rough estimation of the size of the ablation [60] (Figs. 8 and 9A,9B,9C,9D). Furthermore, the echogenic response obscures the margins of the tumor being treated, particularly the posterior margins (Figs. 8 and 9A,9B,9C,9D). Both CT and MR imaging have been reported to be more reliable in this regard [60, 61].
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Regardless of the method used to guide radiofrequency tumor ablation, strategy must be established before placement of the needle. The objective in treating a tumor must be to kill the entire tumor as well as a tumor-free margin of normal liver. The surgery literature has clearly shown that an adequate tumor-free margin is mandatory to prevent local recurrence of a tumor after hepatic resection. In one of the latest publications on the subject, an adequate tumorfree margin was defined as being preferably 2 cm and no less than 1 cm of normal liver [62]. If the goal of radiofrequency ablation is to duplicate the success rate of hepatic resection, then in all likelihood the same requirements for a tumor-free margin will need to be followed.
Given that most radiofrequency ablation devices produce an approximate 3-cm ablation, the largest tumor that should be treated by a single ablation should be smaller than 2 cm in diameter (Fig. 10A). A 2-cm tumor treated with a 3-cm ablation yields at most a 5-mm tumor-free margin. If error in needle placement is factored in, the margin could be much less. Certainly, 3-cm tumors should not be treated by a single 3-cm ablation. To treat a larger tumor, multiple ablations need to be overlapped to build a composite thermal injury of sufficient size to kill the tumor and to provide the desired tumor-free margin. By strict geometric analysis, six overlapping spherical ablations are necessary to create an intact composite thermal sphere of the next magnitude (Fig. 10B). If six 3-cm thermal spheres are precisely overlapped, with four in the x-y plane and two along the z-axis, the largest intact composite thermal sphere that can be created is just 3.75 cm, or 1.25 times the diameter of a solitary sphere. Thus, the largest tumor that should be treated with six 3-cm overlapping ablations should be less than 3.25 cm in diameter. Larger tumors can be treated with radiofrequency ablation, but they require many more ablations or require adjuvant techniques to increase the size of an ablation. A strategy for treating large tumors consists of the creation of thermal cylinders [63] (Fig. 10C).
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When performing multiple radiofrequency ablations using sonographic guidance, it is important to plan the order of ablations so that the deepest ablations are performed before the superficial ones (Figs. 8 and 9A,9B,9C,9D). This strategy minimizes the possibility that microbubbles might obscure visualization of the deeper portions of the tumor and thus prevent completion of the ablation session.
Follow-Up
Immediate evaluation can consist of sonography performed at the time of
treatment. This may be helpful with HCC tumors that are vascular. However, it
may not be helpful in metastatic disease. Solbiati et al.
[58] found that use of
contrast-enhanced sonography may help to detect residual tumor after
radiofrequency treatment. This immediate feedback can be used for
reapplication of radiofrequency in areas that are untreated.
Most institutions perform CT of the liver within a few hours of the ablation to gauge the completeness of the ablation and to look for any potential complications [61]. However, the accuracy of the completeness assessment on the immediate CT scan is often limited because of the presence of an ablation-induced hyperemic rim around the margin of the ablated tissue (Fig. 11A,11B). This hyperemia is difficult to distinguish from residual tumor. Fortunately, the hyperemia is usually resolved by 1 month after the ablation, and a more accurate assessment of the completeness of the ablation can be made at that time (Fig. 12A,12B). In some instances, CT is not performed immediately, but rather 1 month after ablation. If no evidence of residual tumor is seen on the CT scan 1-month after ablation, patients are usually followed up by repeated CT every 3 months. Each follow-up CT scan must be scrutinized for evidence of tumor recurrence in the liver, adjacent to and remote from the ablated site, and outside the liver. Typical sites of extrahepatic tumor recurrence in patients with HCC are the adrenal glands, lungs, bones, and regional lymph nodes along the porta hepatis, gastrohepatic ligament, celiac axis, and cardiophrenic sulcus. Patients with colorectal carcinoma tend to develop extrahepatic metastases at the primary tumor site, in the peritoneal cavity, and in the lungs. Because of the frequency of extrahepatic metastases in patients with colorectal carcinoma, we usually perform both abdominal and pelvic CT every 3 months and chest CT every 6 months.
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The technique used to perform follow-up CT has a significant impact on the
early detection of intrahepatic tumor recurrence. Most early recurrences in
patients with HCC are detected only in the arterial phase of good-quality
three-phase CT. Likewise, the subtle changes of local intrahepatic tumor
recurrence in patients with colorectal metastases may be visualized only
during a strong portal venous phase contrast-enhanced CT scan
[56,
59]. We routinely perform
three-phase CT in all patients with HCC and two-phase CT in patients with
colorectal metastases. Additionally, we obtain repeated -fetoprotein
and carcinoembryonic antigen levels every 3 months in patients with HCC or
colorectal hepatic metastases, respectively. We find the levels helpful in
assessing subtle changes on the CT scans and in determining if additional
evaluation is warranted. Changes in -fetoprotein or carcinoembryonic
antigen values must be assessed on an individual basis for each patient on the
basis of their values before treatment and the normal levels used at each
medical institution.
Several investigators prefer to use MR imaging to follow up their patients after radiofrequency ablation. One study claims that MR imaging is more sensitive than CT for the detection of early intrahepatic tumor recurrence [61]. The interpretation of MR imaging for tumor recurrence is based primarily on the premise that ablated tissue produces minimal signal on T-2 weighted sequences, whereas tumor produces high signal. Dynamic contrast enhancement of suspected tissue is further evidence of tumor recurrence.
Regardless of the technique used to follow up patients after ablation, the primary objective is to detect tumor recurrence as soon as possible so the appropriate therapy can be instituted. If recurrence is limited to the liver, reablation may be effective (Fig. 13A,13B,13C,13D). One of the potential benefits of percutaneous radiofrequency ablation over other more invasive forms of treatment, such as surgery, intraoperative cryotherapy, or intraoperative radiofrequency treatment, is that it can be repeated as often as necessary to treat intrahepatic tumor recurrence. In our practices, we have treated individual patients with local tumor recurrences as many as seven times during a 3-year period. Each time the tumor appeared completely destroyed, and the patient had 3-6 months of asymptomatic health between treatments. If a patient develops extrahepatic tumor or extensive intrahepatic tumor, alternative therapies such as systemic chemotherapy or hepatic chemoembolization should be considered.
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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Percutaneous Treatment of HCC
At least four series document the results of percutaneous radiofrequency
treatment of HCC. The original study of Rossi et al.
[56] used a conventional
needle that was insulated to the distal tip. Rossi et al.
[55] conducted a later series
using an umbrella-type needle (Fig.
3A,3B,3C).
Livraghi et al. [53] and
Francica and Marone [49]
published one study each in which they used a cooled needle device. In all
studies, near-complete necrosis of 90% of the treated tumors had occurred at 6
months. These results were for tumors smaller than 3 cm. However, for the
study by Livraghi et al. [53]
with tumors larger than 3 cm (mean, 5.4 cm,) the complete necrosis rate was
only 47.6%. Complete necrosis was 71% for noninfiltrating tumors that were
3.1-5.0 cm, and only 25% for noninfiltrating tumors greater than 5 cm in
diameter. Also, the rate of disease-free survival at follow-up was lower; the
first study of Rossi et al.
[56] found 64% at 23 months
and 71% at 12 months in a subsequent study
[55]. Francica and Marone
reported 67% of patients to be disease-free at 15 months. Thus, with HCC,
although there is a high rate of complete necrosis of ablated tumors, about a
third of the patients develop recurrent tumor. Kainuma et al.
[50] found it useful to
monitor and perform reablation in these patients. These results are summarized
in Table 1.
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Percutaneous Treatment of Metastatic Liver Tumors
Radiofrequency ablation has also been used to treat tumors that have
metastasized to the liver. The results of five series are summarized in
Table 2. The original study by
Rossi et al. [56] used a
conventional needle that was not insulated to the distal tip. Solbiati et al.
[57] and Livraghi et al.
[54] conducted series with a
conventional needle not insulated at the tip combined with saline infusion.
Ten to fifteen milliliters of saline was introduced into the tumor before
radiofrequency was applied in hopes of increasing the area of tumor necrosis.
Rossi et al. [55] performed a
series using an umbrella-type needle. Solbiati et al.
[59] and Lencioni et al.
[51] reported results using a
cooled-tip needle in 1997. The rate of complete necrosis in these studies
ranged from 52% to 93%. However, few patients remained disease-free; the rates
ranged from as low as 11% at 11 months in the series of Rossi et al.
[56] to as high as 33% at 18
months in the series of Solbiati et al.
[59]. The marked discrepancy
between the complete tumor necrosis rate and the percentage of patients who
remain disease-free is in part due to the biology of metastatic liver disease
and our limited ability to detect the full hepatic tumor burden. Most patients
with a few 2- to 3-cm liver metastases also have numerous subcentimeter or
microscopic tumors that are not detectable with current imaging
technology.
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Laparoscopic Results
Siperstein et al. [45]
described results of laparoscopic radiofrequency ablation of 13 neuroendocrine
tumors in the livers of six patients. The tumors ranged in size from 1 to 7
cm. Follow-up CT showed complete necrosis in 11 of 11 lesions in four patients
at 3 months. All patients showed improvement in their symptoms after
radiofrequency ablation. Cuschieri et al.
[46] used laparoscopic
sonography to guide treatment of 10 patients, two with hepatoma and eight with
metastases. No complications occurred. Patients were discharged within 2 days
of intervention. This compares with the usual same-day discharge after
percutaneous techniques, but it is a shorter hospitalization than with open
techniques. At follow-up ranging from 6 to 20 months, one patient had died of
progressive disease, one patient had further metastases, and eight were
disease-free.
Intraoperative Results
Elias et al. [64] described
the use of combined liver resection and radiofrequency ablation to treat seven
patients with liver metastasis. This is an interesting approach in that these
were liver metastases that were thought to be unresectable by previous
approaches. Radiofrequency was used to ablate those lesions that could not be
surgically resected. The Pringle maneuver was performed in all patients, and
all seven patients were disease-free up to 10-months of follow-up. Jiao et al.
[65] reported a series of
eight patients with HCC and 27 patients with metastases in which 30 of the 35
patients underwent intraoperative radiofrequency ablation using the Pringle
maneuver. Thirteen of the 30 patients had combined radiofrequency ablation and
a surgical resection. At approximately 10 months of follow-up, 24 of the 35
patients were found to have stable disease.
To our knowledge, the largest series to date of intraoperative radiofrequency ablation of hepatic tumors is by Curley et al. [42]. In that study, radiofrequency ablation was used to treat 169 tumors in 123 patients. Of the 123 patients, 92 (75%) were treated with laparotomy and 31 (25%) were treated percutaneously. Forty-eight (39%) patients had HCC and 75 patients (61%) had hepatic metastases. All tumors were treated with an umbrella-type electrode, and a Pringle maneuver was used on all intraoperative cases. Overall, complete necrosis had occurred in 98% of the ablated tumors at a median follow-up of 15 months, and 72% of the patients remained tumor-free during the same time. In the series of Curely et al., the size of the tumors treated by percutaneous radiofrequency (2.4 cm diameter) was less than size of tumors treated intraoperatively (3.8 cm). Those authors did not analyze the outcome difference in the percutaneous and the intraoperative groups. However, only three (1.8%) of 169 treated lesions had local recurrence.
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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As reported with other types of tumor ablation procedures (chemoembolization and cryoablation), a percentage of patients (in our experience, about 25%) will develop a delayed syndrome after ablation. The frequency, severity, and time to onset appear to be directly related to the amount of tissue ablated. The typical presentation consists of flulike symptoms (low-grade fever [up to 38.8°C] accompanied by general malaise) that begin 3-5 days after the ablation and persist for approximately 5 days. With large-volume ablatioons we have seen the syndrome begin almost immediately, cause fever as high as 39.4°C, produce severe lethargy, and last for as long as 2-3 weeks. Several patients have reported night sweats. Appropriate treatment of the syndrome is primarily supportive. We inform patients that they may develop the syndrome after their ablation. Their fever is treated with oral acetaminophen. They are instructed to call us if their fever exceeds 38.8°C or lasts longer than 5 days. If their fever exceeds 38.8°C, a blood sample is drawn and cultured to determine if the patient is septic [66].
Radiofrequency ablation of the liver is considered safe, with an extremely low major complication rate observed by multiple groups. More serious complications have been reported in the literature. Rossi et al. [56] described capsular necrosis, and Solbiati et al. [57, 59] reported intraperitoneal hemorrhage that did not require transfusion. Solbiati et al. [57] also reported one case of fairly severe hypotension that persisted for 3-4 hr after the procedure. Livraghi et al. [53, 54] reported complications in their patients that consisted of two pleural effusions, a perihepatic hematoma, a hemothorax that required surgical repair, self-limited intraperitoneal bleeding, and hemobilia and cholecystitis in one patient each. We have experienced several complications, including three cases of intrahepatic arterial bleeding, with one requiring selective arterial embolization; one burn of the diaphragm that caused pain for 3 monts; one 3-cm hepatic abscess that was treated with oral antibiotics; five 1- to 3-cm first- or second-degree burns along the edge of the grounding pads; and three instances of tumor seeding along the needle tract. Additionally, Lees and Gilliams [67] reported hepatic abscesses and a thermal burn of the transverse colon. Livraghi et al. [52] reported a single death (0.8% rate) in their series. This was the result of a Staphylococcus aureus infection that developed 3 days after the procedure. Because of this complication, those authors administer antibiotic prophylaxis of 1000 mg of ceftriaxone sodium (Rocephin; Roche Laboratories) to all patients.
Few reports mention complications occuring after radiofrequency ablation performed via a laparotomy. Of those that have been reported, most consist of fever and pain. Other reported complications include a perihepatic abscess and an intrahepatic hemorrhage that required arterial embolization [42].
Discussion and Future Strategies
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
|---|
Understanding tissue response to radiofrequency electrocautery application is also important. For example, the complete ablation rate of HCC using percutaneous methods is about 90% [49, 53, 55, 56]. The success rate for metastatic liver disease is much lower [54, 57, 59]. The decreased success of radiofrequency ablation of metastatic liver disease compared with HCC is multifactorial. The reasons include, among other things, inadequate tumor treatment and different tissue responses to radiofrequency treatment. It has been theorized that in HCC tumor necrosis is more uniform and complete, with the margin of ablation being limited by the tumor capsule. Fortunately, tumor invasion beyond the tumor capsule is uncommon; consequently, the chance of local tumor recurrence because of missed tumor is uncommon. However, the margin of metastatic tumors is different, and local invasion of the surrounding hepatic parenchyma is common. Thus, a more aggressive approach to the ablation of metastatic tumor is required to minimize local tumor recurrence.
The need to create a surgical margin to prevent local tumor recurrence restricts successful treatment to smaller lesions. However, advances will probably allow larger volumes of tissue necrosis with radiofrequency ablation. Creation of a larger volume of tissue coagulation will ensure successful ablation of small tumors and allow us to treat patients with larger tumors who may have previously been excluded from consideration for radiofrequency therapy. Furthermore, successful ablation of all tumors may be improved in the future using MR imaging guidance or sonographic contrast agents to determine if tumor margins have been adequately treated [58, 61].
Future strategies may be aimed at changing the tumor response to radiofrequency treatment. For instance, radiofrequency tumor ablation can be increased by stopping blood flow to the tumor. Because flowing blood cools the radiofrequency thermal process, stopping the flow can potentiate an ablation. This can be performed using several methods. The Pringle maneuver can be performed intraoperatively by temporary occlusion of the portal vein and the hepatic artery. This maneuver decreases blood supply to the entire liver and the tumor, thus increasing the size of an ablation. Patterson et al. [69] showed in vivo increased liver necrosis from 6.5 cm3 with radiofrequency ablation compared with 35.0 cm3 with radiofrequency ablation and the Pringle maneuver. This process has been successfully used intraoperatively to treat both HCC and liver metastases [42]. In HCC the main supply to the tumor is via the hepatic artery. If the hepatic artery is embolized before radiofrequency treatment, a larger volume of tissue necrosis will occur [70,71,72,73]. Most research to date has combined intraarterial chemoembolization with percutaneous injection of ethanol [70,71,72]. However, Buscarini et al. [71] and Rossi et al. [73] used chemoembolization or hepatic arterial occlusion in combination with percutaneous radiofrequency ablation for the treatment of HCC. Kainuma et al. [74] used combined intraarterial infusion chemotherapy and radiofrequency thermal ablation to treat colon cancer. Thus, approaches directed at combining radiofrequency ablation with infusion chemotherapy, chemoembolization, or temporary occlusion of the tumor blood supply may improve complete tumor necrosis of small tumors and aid in the treatment of large tumors.
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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TopIntroductionBackgroundEquipmentClinical ApplicationResultsComplicationsDiscussion and Future StrategiesSummaryReferences |
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R. S. Montgomery, A. Rahal, G. D. Dodd III, J. R. Leyendecker, and L. G. Hubbard Radiofrequency Ablation of Hepatic Tumors: Variability of Lesion Size Using a Single Ablation Device Am. J. Roentgenol., March 1, 2004; 182(3): 657 - 661. [Abstract] [Full Text] [PDF]
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M. Fuss and C. R. Thomas Jr. Stereotactic Body Radiation Therapy: An Ablative Treatment Option for Primary and Secondary Liver Tumors Ann. Surg. Oncol., February 1, 2004; 11(2): 130 - 138. [Abstract] [Full Text] [PDF]
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T. J. Vogl, R. Straub, K. Eichler, O. Sollner, and M. G. Mack Colorectal Carcinoma Metastases in Liver: Laser-induced Interstitial Thermotherapy--Local Tumor Control Rate and Survival Data Radiology, February 1, 2004; 230(2): 450 - 458. [Abstract] [Full Text] [PDF]
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 M. P. Goetz, M. R. Callstrom, J. W. Charboneau, M. A. Farrell, T. P. Maus, T. J. Welch, G. Y. Wong, J. A. Sloan, P. J. Novotny, I. A. Petersen, et al. Percutaneous Image-Guided Radiofrequency Ablation of Painful Metastases Involving Bone: A Multicenter Study J. Clin. Oncol., January 15, 2004; 22(2): 300 - 306. [Abstract] [Full Text] [PDF]
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D. Choi, H. K. Lim, M. J. Kim, S. H. Lee, S. H. Kim, W. J. Lee, J. H. Lim, J.-W. Joh, and Y. I. Kim Recurrent Hepatocellular Carcinoma: Percutaneous Radiofrequency Ablation after Hepatectomy Radiology, January 1, 2004; 230(1): 135 - 141. [Abstract] [Full Text] [PDF]
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M. Kitamoto, M. Imagawa, H. Yamada, C. Watanabe, M. Sumioka, O. Satoh, M. Shimamoto, M. Kodama, S. Kimura, K. Kishimoto, et al. Radiofrequency Ablation in the Treatment of Small Hepatocellular Carcinomas: Comparison of the Radiofrequency Effect With and Without Chemoembolization Am. J. Roentgenol., October 1, 2003; 181(4): 997 - 1003. [Abstract] [Full Text] [PDF]
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A. R. Henn, E. A. Levine, W. McNulty, and R. J. Zagoria Percutaneous Radiofrequency Ablation of Hepatic Metastases for Symptomatic Relief of Neuroendocrine Syndromes Am. J. Roentgenol., October 1, 2003; 181(4): 1005 - 1010. [Abstract] [Full Text] [PDF]
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 M. P. Rao and R. Bell Pulmonary Hemorrhage After Radioablation of Liver Metastases Anesth. Analg., September 1, 2003; 97(3): 684 - 686. [Abstract] [Full Text] [PDF]
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A. Giorgio, L. Tarantino, G. de Stefano, V. Scala, G. Liorre, F. Scarano, A. Perrotta, N. Farella, V. Aloisio, N. Mariniello, et al. Percutaneous Sonographically Guided Saline-Enhanced Radiofrequency Ablation of Hepatocellular Carcinoma Am. J. Roentgenol., August 1, 2003; 181(2): 479 - 484. [Abstract] [Full Text] [PDF]
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S. N. Goldberg, J. W. Charboneau, G. D. Dodd III, D. E. Dupuy, D. A. Gervais, A. R. Gillams, R. A. Kane, F. T. Lee Jr, T. Livraghi, J. P. McGahan, et al. Image-guided Tumor Ablation: Proposal for Standardization of Terms and Reporting Criteria Radiology, August 1, 2003; 228(2): 335 - 345. [Abstract] [Full Text] [PDF]
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W. W. Mayo-Smith, D. E. Dupuy, P. M. Parikh, J. A. Pezzullo, and J. J. Cronan Imaging-Guided Percutaneous Radiofrequency Ablation of Solid Renal Masses: Techniques and Outcomes of 38 Treatment Sessions in 32 Consecutive Patients Am. J. Roentgenol., June 1, 2003; 180(6): 1503 - 1508. [Abstract] [Full Text] [PDF]
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C. L. Scaife, S. A. Curley, F. Izzo, P. Marra, P. Delrio, B. Daniele, F. Cremona, J. E. Gershenwald, J. L. Chase, R. D. Lozano, et al. Feasibility of Adjuvant Hepatic Arterial Infusion of Chemotherapy After Radiofrequency Ablation With or Without Resection in Patients With Hepatic Metastases From Colorectal Cancer Ann. Surg. Oncol., May 1, 2003; 10(4): 348 - 354. [Abstract] [Full Text] [PDF]
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R. L. Titton, P. C. Gryzenia, D. A. Gervais, R. S. Arellano, G. W. Boland, and P. R. Mueller Continuous High-Output Drainage of Hepatic Abscess 3 Months After Radiofrequency Ablation of Hepatocellular Carcinoma Am. J. Roentgenol., April 1, 2003; 180(4): 1079 - 1084. [Full Text] [PDF]
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 M. M. Sackenheim Radio Frequency Ablation: The Key to Cancer Treatment Journal of Diagnostic Medical Sonography, March 1, 2003; 19(2): 88 - 92. [Abstract] [PDF]
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S. Chopra, G. D. Dodd III, M. P. Chanin, and K. N. Chintapalli Radiofrequency Ablation of Hepatic Tumors Adjacent to the Gallbladder: Feasibility and Safety Am. J. Roentgenol., March 1, 2003; 180(3): 697 - 701. [Abstract] [Full Text] [PDF]
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T. Livraghi, L. Solbiati, M. F. Meloni, G. S. Gazelle, E. F. Halpern, and S. N. Goldberg Treatment of Focal Liver Tumors with Percutaneous Radio-frequency Ablation: Complications Encountered in a Multicenter Study Radiology, February 1, 2003; 226(2): 441 - 451. [Abstract] [Full Text] [PDF]
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D. Schmidt, J. Trubenbach, J. Brieger, C. Koenig, H. Putzhammer, S. H. Duda, C. D. Claussen, and P. L. Pereira Automated Saline-Enhanced Radiofrequency Thermal Ablation: Initial Results in Ex Vivo Bovine Livers Am. J. Roentgenol., January 1, 2003; 180(1): 163 - 165. [Full Text] [PDF]
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H. Rhim, K.-H. Yoon, J. M. Lee, Y. Cho, J.-S. Cho, S. H. Kim, W.-J. Lee, H. K. Lim, G.-J. Nam, S.-S. Han, et al. Major Complications after Radio-frequency Thermal Ablation of Hepatic Tumors: Spectrum of Imaging Findings RadioGraphics, January 1, 2003; 23(1): 123 - 134. [Abstract] [Full Text] [PDF]
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B.S. Langenhoff, W.J.G. Oyen, G.J. Jager, S.P. Strijk, Th. Wobbes, F.H.M. Corstens, and T.J.M. Ruers Efficacy of Fluorine-18-Deoxyglucose Positron Emission Tomography in Detecting Tumor Recurrence After Local Ablative Therapy for Liver Metastases: A Prospective Study J. Clin. Oncol., November 15, 2002; 20(22): 4453 - 4458. [Abstract] [Full Text] [PDF]
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M. R. Callstrom, J. W. Charboneau, M. P. Goetz, J. Rubin, G. Y. Wong, J. A. Sloan, P. J. Novotny, B. D. Lewis, T. J. Welch, M. A. Farrell, et al. Painful Metastases Involving Bone: Feasibility of Percutaneous CT- and US-guided Radio-frequency Ablation Radiology, July 1, 2002; 224(1): 87 - 97. [Abstract] [Full Text]
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A. Marangio, U. Prati, O. Luinetti, E. Brunetti, and C. Filice Radiofrequency Ablation of Colorectal Splenic Metastasis Am. J. Roentgenol., June 1, 2002; 178(6): 1481 - 1482. [Full Text] [PDF]
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S. N. Goldberg Comparison of Techniques for Image-guided Ablation of Focal Liver Tumors Radiology, May 1, 2002; 223(2): 304 - 307. [Full Text] [PDF]
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D. Choi, H. K. Lim, S. H. Kim, W. J. Lee, H.-J. Jang, H. Kim, S. J. Lee, and J. H. Lim Assessment of Therapeutic Response in Hepatocellular Carcinoma Treated With Percutaneous Radio Frequency Ablation: Comparison of Multiphase Helical Computed Tomography and Power Doppler Ultrasonography With a Microbubble Contrast Agent J. Ultrasound Med., April 1, 2002; 21(4): 391 - 401. [Abstract] [Full Text] [PDF]
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T. Yamagami, T. Nakamura, T. Kato, S. Matsushima, S. Iida, and T. Nishimura Skin Injury After Radiofrequency Ablation for Hepatic Cancer Am. J. Roentgenol., April 1, 2002; 178(4): 905 - 907. [Full Text] [PDF]
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D. S. K. Lu, S. S. Raman, D. J. Vodopich, M. Wang, J. Sayre, and C. Lassman Effect of Vessel Size on Creation of Hepatic Radiofrequency Lesions in Pigs: Assessment of the "Heat Sink" Effect Am. J. Roentgenol., January 1, 2002; 178(1): 47 - 51. [Abstract] [Full Text] [PDF]
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T. de Baere, F. T. Lee Jr., A. S. Wright, T. C. Winter III, and D. M. Mahvi Radiofrequency Ablation of the Liver Am. J. Roentgenol., November 1, 2001; 177(5): 1213 - 1215. [Full Text] [PDF]
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G. D. Dodd III, M. S. Frank, M. Aribandi, S. Chopra, and K. N. Chintapalli Radiofrequency Thermal Ablation: Computer Analysis of the Size of the Thermal Injury Created by Overlapping Ablations Am. J. Roentgenol., October 1, 2001; 177(4): 777 - 782. [Abstract] [Full Text] [PDF]
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H. Rhim, S. N. Goldberg, G. D. Dodd III, L. Solbiati, H. K. Lim, M. Tonolini, and O. K. Cho Essential Techniques for Successful Radio-frequency Thermal Ablation of Malignant Hepatic Tumors RadioGraphics, October 1, 2001; 21(90001): S17 - 35. [Abstract] [Full Text] [PDF]
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H. Choi, E. M. Loyer, R. A. DuBrow, H. Kaur, C. L. David, S. Huang, S. Curley, and C. Charnsangavej Radio-frequency Ablation of Liver Tumors: Assessment of Therapeutic Response and Complications RadioGraphics, October 1, 2001; 21(90001): S41 - 54. [Abstract] [Full Text] [PDF]
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S. S. Raman, D. S. K. Lu, D. J. Vodopich, J. Sayre, and C. Lassman Minimizing Diaphragmatic Injury during Radio-frequency Ablation: Efficacy of Subphrenic Peritoneal Saline Injection in a Porcine Model Radiology, March 1, 2002; 222(3): 819 - 823. [Abstract] [Full Text] [PDF]
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T. Shibata, Y. Iimuro, Y. Yamamoto, Y. Maetani, F. Ametani, K. Itoh, and J. Konishi Small Hepatocellular Carcinoma: Comparison of Radio-frequency Ablation and Percutaneous Microwave Coagulation Therapy Radiology, May 1, 2002; 223(2): 331 - 337. [Abstract] [Full Text] [PDF]
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