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Vascular and Interventional Radiology |
1 From the Departments of Radiology (S.G.S., K.T., D.F.A., E.v.S., K.H.Z., D.F.K., F.A.J.) and Surgery (P.R.M.), Brigham and Women’s Hospital, 75 Francis St, Boston, MA 02115. From the 1999 RSNA scientific assembly. Received February 15, 2000; revision requested March 27; revision received May 5; accepted May 22. S.G.S. supported in part by a 1998 Toshiba America/RSNA Seed Grant (1), Galil Medical Systems, and GE Medical Systems. Address correspondence to S.G.S. (e-mail: sgsilverman@partners.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Fifteen hepatic tumors (mean diameter, 2.9 cm) in 12 patients were treated (18 total cryoablations). Fourteen were metastases and one was a hemangioma; all were proved at biopsy. By using a 0.5-T open MR imaging system, cryoneedles were placed and lesions ablated by using real-time monitoring. Clinical signs and symptoms were assessed and laboratory tests performed. Intraprocedural depictions of iceballs were compared with contrast material–enhanced MR imaging–based estimates of cryonecrosis that were obtained 24 hours after cryoablation.
RESULTS: MR imaging–guided percutaneous cryotherapy resulted in no serious complications and no clinically important changes in serum liver enzymes or creatinine or myoglobin levels. Intraprocedural MR imaging demonstrated iceballs as sharply marginated regions of signal loss that expanded and engulfed tumors. The maximal iceball size was 4.9 x 2.2 x 2.2 cm with the use of one cryoneedle and 6.0 x 5.6 x 4.9 cm with three cryoneedles. Intraprocedural iceball depictions correlated well with postprocedural cryonecrosis estimates.
CONCLUSION: MR imaging–guided percutaneous cryotherapy of liver tumors is feasible and safe. MR imaging can be used to estimate cryotherapy effects and guide therapy intraprocedurally.
Index terms: Cryotherapy • Liver neoplasms, therapy, 761.1261 • Magnetic resonance (MR), guidance, 761.121411, 761.12412, 761.121415
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Cryotherapy, the in situ freezing of tissues, has been used successfully in the surgical treatment of primary and secondary hepatic malignancies (2). By using intraoperative ultrasonography (US) to guide cryoprobe placement and monitor iceball formation, cryotherapy of unresectable primary and secondary hepatic malignancies has been performed through a surgical approach for more than a decade (2). Although there is debate as to whether survival is prolonged, when an adequate margin is achieved there is complete ablation of the treated tumor (2). Despite this experience, to our knowledge, to date, cryotherapy had not been used clinically as a percutaneous ablative agent for liver and other deep tissues because the heretofore large cryoprobes were considered dangerous for placement with a percutaneous approach (1).
US monitoring is an advance in the intraoperative cryotherapy of liver tumors. US can depict the effects of freezing in real time and accurately depict the zone of necrosis that cryoablation produces (3). However, because of shadowing behind its proximal edge, the circumference of the iceball cannot be seen on a single view. As a result, assessment of lesion coverage is not possible. Conversely, magnetic resonance (MR) imaging has demonstrated the entire iceball in animal models (4–8). Like those demonstrated at US, MR imaging–demonstrated lesions created by cryoablation (hereafter referred to as "cryolesions") can be used to accurately predict the proximal outer boundary of tissue necrosis within 1–5 mm (8,9); unlike US, MR imaging does not create a shadow artifact and therefore demonstrates the entire circumference of the cryoeffect (6,7,9,10). In addition, it has been speculated that MR imaging may be used to predict temperature distribution within the iceball; this concept could add precision to the monitoring of iceball growth and the effects of cryotherapy (11).
Until now, several obstacles, which included the unavailability of open-configuration MR imaging systems and the lack of MR imaging–compatible cryoprobes, had prevented the use of MR imaging to monitor cryotherapy. Technologic advances now permit the percutaneous delivery of cryotherapy with small needlelike probes. Open-configuration MR imaging systems facilitate needle probe placement and intraprocedural treatment monitoring. Therefore, on the basis of the established effectiveness of cryotherapy in ablating liver tumors, the decreased morbidity of percutaneous approaches, and the advantages of MR imaging in delineating cryolesions, we sought to develop a method of MR imaging–guided percutaneous cryotherapy. The purpose of this study was to describe this method and to evaluate its feasibility and safety in the treatment of liver tumors.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The interventional MR imaging suite also contained an MR imaging–compatible anesthetic delivery system (Narkomed; North American Drager, Telford, Pa). An MR imaging–compatible patient monitoring system included a pulse oximeter, a noninvasive blood pressure monitor, an airway carbon dioxide monitor, and an electrocardiographic device (Datascope MR Monitor; Datascope, Paramus, NJ).
Cryotherapy System
Percutaneous cryotherapy was performed by using a cryotherapy delivery system (Cryohit; Galil Medical, Yokneam, Israel) that had recently been approved by the U.S. Food and Drug Administration. This system consisted of a computer workstation, a gas gauge, a gas distribution system, and accessories that included needlelike cryoprobes, temperature sensors, and a remote control device. It used high-pressure cooling gas (argon), which achieved temperatures as low as -185°C at the tip of the needle probes. The argon was converted to cold low-pressure liquid by using the Joule-Thomson effect (14). To thaw the tissues, a high-pressure gas (helium) was converted to a warm low-pressure gas. The main unit was not MR imaging–compatible and therefore was housed outside the suite. Although the gas could flow directly to the probes, in our suite, the gas flowed through pipes that entered a penetration panel in the wall of the suite, coursed under the floor, and exited directly from the side of the interventional MR imaging system.
The gas was delivered by using biocompatible and MR imaging–compatible cryoprobes (diameter range, 2.1–2.4 mm; length range, 16–20 cm), which were needlelike and had an outer diameter approximating 13–14 gauge; each had approximately the same performance characteristics. The cryoprobes were designed for placement with a trocar technique (Fig 1). Each cryoprobe, hereafter referred to as a "cryoneedle," was equipped with a thermocouple that monitored needle-tip temperature throughout freezing and thawing. A computer interface displayed needle-tip temperatures and could be used to input the desired temperature during the procedure. Heat exchange occurred along only a 4-cm-long segment at the distal end of each cryoneedle. Three cryoneedles could be used simultaneously in one or more locations and frozen or thawed independently.
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All potential participants underwent MR imaging to determine lesion size and number. In patients who had no extrahepatic disease, enrollment was limited to those whose disease was considered technically or medically inoperable or who refused surgery. Patients must have completed chemotherapy, been hemodynamically stable, and had normal or correctable hemostatic parameters, no contraindications to MR imaging, and no history of active ischemic heart disease. Active ischemic heart disease was defined as recent myocardial infarction, recent symptoms of angina, or ischemic changes at electrocardiography. The last criterion was necessary because S-T and T wave segments cannot be monitored at MR imaging and, as such, silent ischemia could go undetected (15,16).
Notice of the activation of the research protocol was circulated to general surgeons, medical oncologists, and abdominal radiology colleagues. During a 12-month period, 37 patients were referred for consideration for MR imaging–guided percutaneous cryotherapy. Of these, 25 were excluded because 11 had lesions that were larger than 5 cm, nine had more than four lesions and after consultation with referring physicians were treated with systemic therapy, and five preferred a different form of therapy.
Twelve of the 37 patients were enrolled, and written informed consent was obtained from all. The preprocedural evaluation included a consultation with an interventional radiologist, a procedural examination with the open-configuration MR imaging system for planning of the approach, and a consultation with an anesthesiologist. Preprocedural laboratory tests included prothrombin and partial thromboplastin time, white blood cell and platelet count, and hematocrit, serum creatinine, aspartate aminotransferase (AST), alanine aminotransferase (ALT), and myoglobin levels.
Procedures
Eighteen cryoablations were performed during 16 treatment procedures for 15 tumors in 12 patients (Table 1). Cryoablation was defined as the freezing of a lesion during a procedure. The largest tumor was 5.0 x 4.7 x 4.5 cm and the smallest was 1.3 x 1.1 x 1.0 cm. Eleven tumors were less than 1 cm from the liver surface and included four less than 1 cm from the diaphragm and two less than 1 cm from the right kidney. All tumors were metastatic except for one. The patient with this tumor presented to us from another hospital with a recently resected abdominal liposarcoma, an MR image demonstrating a liver lesion that was suspicious for metastasis, and a percutaneous biopsy of the lesion that reported metastatic liposarcoma. As per our protocol, biopsy and treatment were performed in the same session. However, after treatment, the diagnosis from our biopsy was hepatic hemangioma.
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By using the MR imaging-guided frameless stereotactic techniques described, an MR imaging–compatible 18-gauge needle (E-Z-Em, Westbury, NY) was inserted into the targeted lesion. MR imaging was used to confirm the position of the needle in three planes. Biopsy material was obtained coaxially through the 18-gauge needle by using MR imaging–compatible 20–22-gauge needles (E-Z-Em). A cryoneedle was placed in tandem alongside the reference biopsy needle by using a trocar technique. Additional cryoneedles (up to three) were placed as needed to treat the tumor. Two freeze-thaw cycles (15-minute freeze, 10-minute thaw) were used in 16 of 18 cryoablations. One freeze-thaw cycle was used in the treatment of two lesions during the same procedure. During freezing, cryoneedle tip temperatures reached a nadir of -140° to -160°C.
MR imaging was performed every 1–3 minutes in at least two planes to monitor cryolesion growth and tumor coverage. The following sequences were used: T1-weighted fast spin-echo (400–750/18–22 [repetition time msec/echo time msec]; echo train length, four; section thickness, 8 mm; field of view, 26–32 cm) in eight cryoablations, spin-echo (300/12; section thickness, 8 mm; field of view, 26 cm) in one cryoablation, T2-weighted fast spin-echo (2,100–3,500/88; echo train length, eight; section thickness, 5 mm; field of view, 28–32 cm) in three cryoablations, and fast spoiled gradient-echo (17–51/4.8–10.0; flip angle, 60°; section thickness, 5–8 mm; field of view, 26–32 cm) in six cryoablations.
Imaging and Laboratory Evaluation
At the end of the procedure, transverse T2-weighted fast spin-echo (3,000–5,000/92; echo train length, eight; section thickness, 10 mm; field of view, 28–32 cm) images were obtained through the liver. Patients were observed in the recovery room for 2 hours and then admitted for up to 24 hours; during this time, they were observed and monitored and blood tests were performed. White blood cell and platelet count and serum hematocrit, AST, ALT, creatinine, and myoglobin levels were obtained at 6, 12, and 24 hours and 1 week after the procedure. Serum prothrombin and partial thromboplastin times were obtained at 6 hours.
Conventional 1.5-T MR imaging was performed at 24 hours to assess complications and define the extent of cryonecrosis. It consisted of transverse T1-weighted spin-echo (600/14; section thickness, 4 mm; field of view, 34 cm), transverse T2-weighted fast spin-echo (5,100/100; echo train length, 12; section thickness, 4 mm; field of view, 30 cm), and transverse fast multiplanar spoiled gradient-echo (285/1.6; flip angle, 75°; section thickness, 5 mm; field of view, 34 cm; with fat suppression) imaging performed before and after the intravenous injection of 20 mL gadopentetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, NJ).
Intraprocedural MR images of iceballs were compared with postprocedural estimates of cryonecrosis, which was defined as new (as compared with findings on pretreatment MR images) areas of decreased enhancement. Volumes and locations of each iceball on MR images acquired intraprocedurally were compared with their corresponding volumes and locations of decreased enhancement on conventional 1.5-T MR images obtained 24 hours postprocedurally. Volumes for each region were estimated by one author (K.T.) by measuring maximum diameters in three planes and by using the formula for the volume of an ellipsoid: (4/3) 
r1 r2 r3, where r1 and r2 are the maximum diameters divided by two and r3 is the length divided by two. The mean volumes in each group were compared by performing a two-sided paired Student t test. Conventional 1.5-T MR images were obtained at 3 months by following the protocol used at 24 hours to further assess the ablation effect.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All patients tolerated the procedure well; 10 of the 12 patients were discharged the day after the procedure and two were discharged on the 2nd day. Ten either denied pain or had mild right upper quadrant abdominal discomfort; in the recovery room, two patients complained of moderate to severe right upper quadrant pain. The pain was controlled with narcotic analgesia and resolved within 1–2 hours. One patient complained of mild self-limited nausea; that is, the nausea resolved by itself without therapy.
In all patients, there were no changes in serum creatinine level and prothrombin and partial thromboplastin times and only mild transient increases in serum ALT and AST levels and white blood cell count. The serum myoglobin level increased slightly and transiently to 151 and 257 µg/L after two procedures (normal range, 0–100 µg/L). Transient mild decreases in hematocrit level were observed in all patients but were unaccompanied by signs or symptoms of hemorrhage. All of these values were normal at 1 week after the procedure. There was a downward trend in platelet counts, but none was less than normal.
One patient developed a self-limited episode of hyperbilirubinemia that was unaccompanied by pain after the treatment of a 2.4-cm lesion in hepatic segment 4. Postprocedural US showed no bile duct dilatation or biloma. The episode was believed to be due to drug-induced cholestasis that was possibly caused by the anesthetic. One patient had transient mild fever. At 1 week after the procedure, no patient reported procedure-related discomfort or symptoms. All patients resumed their usual daily activities, including work, within several days.
The iceballs were seen as sharply marginated, teardrop-shaped or ellipsoid regions of signal loss on fast spin-echo, spin-echo, and gradient-echo MR images (Fig 2). Intraprocedural MR imaging demonstrated iceballs that were distinguished from untreated tumor and gradually "eclipsed" the tumor (Fig 2). The maximal iceball size was 4.9 x 2.2 x 2.2 cm when one cryoneedle was used and 6.0 x 5.6 x 4.9 cm when three cryoneedles were used (Fig 3) (Table 2). As the trial progressed, we used more cryoneedles per cryoablation and achieved larger iceballs (Table 2). Intraprocedural images of iceball locations correlated well with postprocedural estimates of cryonecrosis that was indicated by areas of decreased enhancement at contrast-enhanced MR imaging performed 24 hours after the procedure (Fig 4). The mean intraprocedural cryonecrosis volume was not significantly different from the mean postprocedural iceball volume (P = .86) (Table 3). At contrast-enhanced MR imaging for evaluation of the extent of tumor necrosis 24 hours postprocedurally, 100% of the tumor was necrotic in two of the 15 treated tumors; 75%–99%, in eight; 50%–74%, in one; 25%–49%, in one, and less than 25%, in three.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Our experience suggests that MR imaging–guided percutaneous cryotherapy of liver tumors is feasible and safe. The primary innovation in our technique is that cryotherapy of deep and sizeable hepatic tumors may be performed through a percutaneous route by using small needlelike probes. Preliminary experience with percutaneous cryotherapy by using US in humans (20,21) and CT in pigs (22) has been reported. In the latter report, probes were placed by using the Seldinger technique, the same technique employed during prostate cryotherapy and liver cryosurgery. Our probes were specially designed for placement with a trocar technique, which requires no sheaths, guide wires, or dilators. The probes we used are small enough that their direct insertion was more akin to the placement of a needle. Hence, we termed the instruments "cryoneedles." Despite the concern for hemorrhage that had been raised in surgical reports (2,18,19), no serious bleeding occurred with our technique. Our experience included the cryoablation of hypervascular malignant lesions in multiple patients and a hepatic hemangioma in one patient. The self-limited small hematoma that occurred probably was not related to the cryoablation but rather a result of the multiple cryoneedle passes needed to target a lesion that was difficult to access.
Renal complications of cryosurgery (2) were not observed. Although we used a prophylactic regimen to protect the kidney in the event of myoglobinuria, serum myoglobin levels did not increase substantially. In one of the patients with a mild increase in serum myoglobin level, the cause may have been freezing of the adjacent diaphragm (Fig 5). Notwithstanding the aforementioned safety of our procedures, most reported complications at cryosurgery result from the treatment of large or multiple tumors (2). The lack of complications in our series may have been due in part to the relatively small size of the patients’ tumors.
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The second main innovation in our technique was the use of open-configuration MR imaging for guidance and thermal monitoring. By using an open-configuration MR imaging system with an integrated guidance mechanism, the entire procedure was performed in one setting rather than placing the cryoneedles under CT or US guidance and then taking the patient to MR imaging for monitoring. The MR imaging–compatible cryoneedles were well visualized throughout the procedure. Another benefit of MR imaging guidance was having the ability to reposition the cryoneedles on the basis of the results of imaging during cryotherapy. On the basis of views of the developing iceball and its relationship to the tumor, we repositioned the cryoneedles as necessary. With regard to thermal monitoring, MR imaging demonstrated the entire iceball, as shown in animal models (4–8). The short T2 relaxation time of ice results in excellent images of the iceball or cryolesion, which, when either T1- or T2-weighted sequences are used, is represented as a signal void (4–8). By using a variety of pulse sequences, excellent contrast between the iceball and tumor can be achieved in either a multiplanar or three-dimensional format. Multidimensional imaging allows accurate demonstration of the iceball and its relationship to the treated tumor (4–8).
Although the use of T2-weighted sequences increased contrast between the bright tumor and the dark iceball (Fig 2), lesion-to-background contrast was sufficiently high to allow T1-weighted spin-echo or fast spoiled gradient-echo imaging, which enabled shorter acquisition times (Fig 3). Intraprocedural T2-weighted MR imaging immediately following cryoablation demonstrated the volume of treated tissue, which was depicted as a region of high signal intensity (Fig 2d). This signal intensity may have been due to edema that was caused by leaky capillaries and/or to increased extracellular water that was caused by thawed ice. The tumor may also still be seen if its native T2 value is sufficiently high. When this occurs, treatment margins can be assessed.
Consistent with the results of animal studies (8), intraprocedural depictions of iceballs correlated well with postprocedural estimates of necrosis. Visualizing ablative changes intraprocedurally obviates 24-hour MR imaging or CT. This is important because, although tumor ablation with ethanol injection, radio frequency, and interstitial laser therapy is performed with imaging guidance, the amount of tissue change demonstrated at US and CT during these therapies is limited and variable and does not accurately reflect the zone of necrosis (23). In our series, intraprocedural MR imaging accurately depicted the changes seen at 24 hours.
CT has been suggested as a means to guide percutaneous cryotherapy (22,24). However, CT scans depicting iceballs as well-marginated low-attenuating zones cannot be differentiated from most liver tumors, which also are hypoattenuating. Therefore, it may be difficult to assess lesion coverage intraprocedurally. CT assessment is limited to the transverse plane, and, despite the availability of CT fluoroscopy, radiation dosimetry considerations prohibit any real- or semi–real-time assessment of tumor coverage.
There are disadvantages to our technique in its current form; general anesthesia might be considered one. We used general anesthesia for two main reasons. First, because long procedure times are often needed in the early development of new techniques, our procedures (including the total time the patient was in the room) lasted 3–6 hours—too long for patients under conscious sedation to tolerate. Second, imaging required a mean of 60 seconds of breath holding, which was difficult for many patients to perform, particularly when performed repeatedly. However, we intend to use intravenous conscious sedation when imaging and procedure times are reduced sufficiently. Our results support the eventual performance of the procedure on an outpatient basis.
We were unable to achieve complete ablation in several cases. Although we attempted to treat all lesions completely, we erred on the side of caution to first prove that percutaneous cryotherapy is feasible and safe. As we became more comfortable with the technique, we used more cryoneedles per lesion and provided better lesion coverage as the trial progressed (Table 2). Depicting the ablative effect distinctly and clearly with MR imaging at least affords the ability to carry out the ablation to a full extent and with the confidence that nearby structures will not be harmed.
In conclusion, a method of ablating liver tumors with cryotherapy has been described. The rationale for MR imaging-guided percutaneous cryotherapy of liver tumors is summarized: Freezing is an effective ablative technique and can be monitored well with MR imaging. Unlike those after heating, the margins of necrosis following cryoablation are sharp and unambiguous, and the MR imaging–depicted boundaries of the treatment correlate well with necrosis. MR imaging, like US, is near real time and multiplanar; unlike US, it can depict the entire iceball and surrounding structures, and the iceball can be discriminated from tumor during the procedure. We have demonstrated that percutaneous cryotherapy of liver tumors is feasible and safe, and MR imaging can be used intraprocedurally to depict cryolesions as well-marginated signal voids that are clearly distinguishable from untreated tumor and correlate well with 24-hour MR imaging–based estimates of necrosis. Although this method requires refinement and further assessment, MR imaging-guided percutaneous cryotherapy appears to be a feasible method with advantages to add to the growing list of radiologic methods for tumor ablation.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, S.G.S., K.T.; study concepts, S.G.S., K.T., D.F.A., E.v.S., K.H.Z., F.A.J.; study design, S.G.S., K.T., D.F.A., K.H.Z., F.A.J.; definition of intellectual content, S.G.S., K.T., D.F.A., E.v.S., K.H.Z., F.A.J.; literature research, S.G.S., K.T., P.R.M.; clinical studies, S.G.S., K.T., D.F.A., E.v.S., D.F.K., P.R.M.; data acquisition, S.G.S., K.T., D.F.A., D.F.K., P.R.M.; data analysis, S.G.S., K.T., D.F.A., K.H.Z.; statistical analysis, K.H.Z.; manuscript preparation, S.G.S., K.T., D.F.A., E.v.S., D.F.K., P.R.M., F.A.J.; manuscript editing, S.G.S., K.T., D.F.A., E.v.S., F.A.J.; manuscript review, all authors.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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