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DOI: 10.1148/radiol.2413051526
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(Radiology 2006;241:746-752.)
© RSNA, 2006


Experimental Studies

MR-guided Radiofrequency Ablation: Do Magnetic Fields Influence Extent of Coagulation in ex Vivo Bovine Livers?1

Christina Schraml, MD, Christophe Aubé, MD, Hansjoerg Graf, PhD, Andreas Boss, MD, Stephan Clasen, MD, Tina Herberts, PhD, Diethard Schmidt, MD, Fritz Schick, MD, PhD, Claus D. Claussen, MD and Philippe L. Pereira, MD

1 From the Department of Diagnostic Radiology, University Hospital of Tuebingen, Hoppe-Seyler-Str 3, 72076 Tuebingen, Germany. Received September 12, 2005; revision requested November 10; revision received December 23; accepted January 24, 2006; final version accepted March 20. Supported by Radionics Europe Valleylab. C.S. supported by the German Ministry for Education and Research (contract no. 16SV1351). Address correspondence to P.L.P. (e-mail: philippe.pereira{at}med.uni-tuebingen.de).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Purpose: To prospectively determine if static magnetic fields of magnetic resonance (MR) imagers affect radiofrequency (RF) ablation coagulation volume and shape.

Materials and Methods: Ex vivo RF ablations of bovine livers were performed with magnetic field strengths of 0.2, 1.5, and 3.0 T and were compared with ablations performed outside the magnetic field in a control group. Two MR-compatible monopolar RF devices (internally cooled single and cluster electrodes) were systematically tested. Length of long axis (y-axis), length of two short axes (x- and z-axes), and coagulation volume and shape measured outside and inside different magnetic fields were compared with the Dunnett test. Significance level was set to .05.

Results: For the single electrode, no significant difference was observed between length of short axes and coagulation volume and shape measured inside and outside the magnetic field. Mean x- and z-axis lengths were 2.3 and 2.6 cm, respectively, outside the magnetic field; 2.4 and 2.4 cm, respectively, at 0.2 T; 2.5 and 2.6 cm, respectively, at 1.5 T; and 2.2 and 2.5 cm, respectively, at 3.0 T. Differences between length of long axis, length of short axis perpendicular to static magnetic field, and coagulation volume and shape achieved with the cluster electrode inside and outside the magnetic field were not significant. Mean x- and z-axis lengths were 3.9 and 3.9 cm, respectively, outside the magnetic field; 3.7 and 3.8 cm, respectively, at 0.2 T; 4.0 and 4.3 cm, respectively, at 1.5 T; and 3.8 and 3.8 cm, respectively, at 3.0 T. Differences between ablations performed at 1.5 T and those performed in the control group with the cluster electrode were significant (P = .026). In this case, a difference of 4 mm in the length of the short axis parallel to the magnetic field was detected, but there was no significant difference in coagulation volume.

Conclusion: No significant differences in coagulation volume and shape could be recorded between RF ablations performed outside and those performed inside the static magnetic field.

© RSNA, 2006


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Magnetic resonance (MR) imaging–guided percutaneous radiofrequency (RF) ablation is used for minimally invasive interstitial thermotherapy of neoplastic tissue and has gained importance in recent years (15). MR guidance offers considerable advantages for RF ablation: It provides true multiplanar imaging capabilities, high intrinsic soft-tissue contrast, and adequate vascular conspicuity (6). Compared with other imaging modalities, MR imaging offers the unique advantage of being able to depict the zone of irreversible tissue damage by means of T2-weighted MR imaging immediately after ablation; thus, the RF probe is still in place (7). This capability is not provided with computed tomography (CT) or ultrasonography (US) because the coagulation zone and tumor have similar signal intensity patterns at CT and because US is hampered by hyperechoic steam bubbles caused by thermal tissue heating. Additionally, MR thermometry enables physicians to monitor RF ablation with temperature maps; these maps enable healthy tissue at the circumference of the ablation target to be distinguished from tissue with thermal damage (8,9).

The physical principle of RF ablation is based on ionic agitation in an alternating electric field. Electric energy is converted into heat inside the tissue surrounding the tip of the active electrode. If RF ablation is performed inside a strong magnetic field (ie, inside the static magnetic field of the MR imager), charged particles such as Na+ and Cl ions may be affected by the Lorentzian force. Moving ions with a velocity component perpendicular to the magnetic field are directed to a spiral path. An additional electric tissue resistance (known as the Hall resistance) occurs owing to the spiral ion current pathways. This effect depends on the direction of current flow in relation to the direction of the magnetic field (Fig 1). The number of charge carriers in the human body is lower than that in metals; therefore, electrolytic conduction in the human body is affected more than electrical conduction in metals (10). For comparison, charge carrier density is 1017 per cubic millimeter in 140 mmol of NaCl and 1020 per cubic millimeter in metal. Subsequently, the spatial distribution of tissue resistance might be substantially changed compared with that in the free-field case. Thus, the extent and shape of RF-induced coagulation may vary when ablations are performed inside a magnetic field because of the different spatial distribution of electrical resistance in the tissue around the electrode tip.


Figure 1
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Figure 1: Schematic drawing shows influence of magnetic field strength on spatial distribution of resistance. Current flows between the active electrode and the grounding pad, as indicated by the electric flux lines of the electric field (E). Current paths perpendicular to the magnetic field B0 are strongly affected, whereas current paths parallel to B0 are not influenced. Thus, geometry of coagulation necrosis may be altered if RF ablation is performed inside a clinical MR imager.

 
For successful therapy, it is necessary to achieve a predefined extent of tissue coagulation. Results of a preliminary study indicate there is a possible decrease in coagulation volume when RF ablations are performed with MR guidance (11). Thus, the aim of our study was to prospectively determine if static magnetic fields of MR imagers affect RF ablation coagulation volume and shape.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Our study received support from the German Ministry for Education and Research (contract no. 16SV1351), which provided financial support to an author (C.S.); Siemens Medical Solutions (Erlangen, Germany), which provided continuous intellectual support concerning MR technology; and Radionics Europe Valleylab (Boulder, Colo), which provided material and continuous intellectual support. All authors had full control of the study data and information submitted for publication. No authors are employees of or consultants for the organizations that provided support.

Experimental Setting
Experiments were performed with three field strengths because RF ablation may be performed with clinical MR imagers with field strengths that vary from low (0.2 T) to high (3.0 T).

Ablation systems.—Internally cooled MR-compatible electrodes were used with the RF device (Cool Tip; Valleylab, Boulder, Colo). Experiments were performed with two electrode types (an internally cooled single electrode and a cluster electrode) to determine whether different values of transferred energy would be affected differently by the magnetic field. The single electrode has a 3-cm-long active distal part and requires two grounding pads in the clinical routine. The cluster electrode consists of three parallel internally cooled single electrodes with a 1.6-mm diameter spaced 0.5 cm apart and grouped equidistantly in a triangle. Each electrode has a 2.5-cm-long active (noninsulated) distal part. Four grounding pads are required for use of the cluster electrode in each clinical application. Both the cluster electrode and the single electrode of this RF system use the same generator with a maximum power output of 200 W.

Experimental setup and study design.—RF ablations performed in ex vivo bovine livers have been shown to generate reproducible results (3). To avoid interexaminer differences, all experiments were performed by one examiner (C.S.), who used freshly excised bovine livers purchased from a local butcher. The liver was cut into 10 x 10 x 10-cm blocks. When dissection after RF ablation showed that a block contained parts of large (>3 mm in diameter) vessels, the block was excluded from evaluation because the presence of large vessels, even those without perfusion, may markedly influence the geometry of coagulation necrosis in ex vivo experiments (12). In these cases, ablation was repeated to obtain a total of six ablations for each group. In total, six livers were needed.

To avoid field distortion from metallic devices, RF ablation inside and outside the magnetic field was performed inside a plastic container filled with a conductive physiologic 0.9% NaCl solution (Fig 2). Livers and NaCl solution had a predefined mean temperature of 20°C ± 2 (standard deviation). Temperature was measured with a fluoroptic thermometer (LXT Luxtron One; Luxtron, Santa Clara, Calif). For ex vivo experiments, only one 15.5 x 70.0 x 0.05-mm grounding pad (Tyco Healthcare Group, Boulder, Colo) was used. It was fixed laterally inside the container at a distance of 15 cm from the active RF applicator. In all cases, the grounding pad was fixed parallel to the B0 orientation of the magnetic field. The applicator electrodes were positioned upright in the center of the liver block. The axis of the electrode shaft was parallel to the plane of the grounding pad.


Figure 2
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Figure 2: Schematic drawing shows experimental setup. The liver block was immersed in a tank filled with a 0.9% NaCl solution to ensure electrical conductivity. The grounding pad was fixed laterally inside the tank. The orientation of the active electrode and the grounding pad in relation to the magnetic field B0 are shown.

 
RF ablations were repeated at 0.2 T, 1.5 T, and 3.0 T (n = 6) and were compared with ablations performed outside the magnetic field (n = 6). The same ablation protocol was used for both the monopolar single electrode (24 ablations) and the monopolar cluster electrode (24 ablations). In total, 53 liver blocks were evaluated; five blocks were excluded because of an irregularly shaped zone of induced coagulation that was due to the presence of large vessels. In consideration of coagulation volume dimension and variance in preliminary ex vivo experiments, an evaluation of sample size based on the results of t tests was performed before the experiments were conducted. According to the values of variance, a sample size of six experiments per group was necessary, provided the significance niveau was set to 2%.

Ablation protocols.—An RF generator was first placed outside the MR imaging room in the control room for all experiments. To exclude effects due to different cable systems, the same 8-m-long MR-compatible cable was used to perform ablation outside the magnetic field. Cable loops were avoided to reduce differences in energy transfer caused by electrical induction. To exclude the influence of heat or mechanical wear, the needle and grounding pad in use were changed after every six ablations. Furthermore, the NaCl solution was also replaced after six ablations. The standard protocol recommended by the manufacturer was successfully implemented for each ablation: RF current was emitted for 12 minutes, with the generator set to deliver the maximum power with the impedance control method (13,14).

Assessment of coagulation volume and shape.—For all comparative measurements, only white coagulation was assessed because it represented the zone in which complete cellular destruction was ensured (15). To perform a more precise analysis of the coagulation geometry, the coagulation size was assessed in three dimensions in space. To avoid interexaminer differences, the same examiner (C.S.) assessed coagulation size. After ablation, the liver blocks were dissected in the longitudinal plane without removal of the electrode in order to cut precisely along the long axis. Long axis (y-axis) and short axis (z-axis) were measured, with only the central white coagulation taken into account (Fig 3). The liver was then cut transversely (perpendicular to the longitudinal plane), and the second short axis (x-axis) was assessed (Fig 4).


Figure 3
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Figure 3: Photograph shows coagulation necrosis. This sample was obtained with the internally cooled single electrode (control group) after the first cut along the active electrode shaft and parallel to the grounding pad. The track of the needle is visible in the middle of the coagulation; carbonization (black arrows), white coagulation area (*), and red zone of coagulation necrosis (white arrows) are also visible. In this study, only the white zone of coagulation was taken into account for measurements.

 

Figure 4
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Figure 4: Schematic drawing shows assessment of coagulation dimensions. Long axis (y-axis) and two short axes (x and z axes) in two planes were assessed. For better analysis of possible changes in coagulation symmetry, both short axes, as well as the distances (x1, x2; z1, z2) from the needle track, were measured. The grounding pad was orientated parallel to the y-z plane, and the magnetic field was orientated in the z direction.

 
Deviation of current flow can modify the shape of necrosis. Thus, the shape of coagulation was assessed by measuring both short axes (x and z axes). Furthermore, the complete diameter of the coagulation zone and each distance from the needle track (x1, x2, z1, and z2) were assessed (Fig 4). Thus, possible changes in coagulation geometry could be identified by comparing the values of the difference for x1 minus x2 and for z1 minus z2 at different field strengths.

The ablation area volume was calculated by using the same formula used to calculate ellipsoidal volume: (1/6{pi}) · LS1 · LS2 · Ll, where LS1 is the length of short axis 1, LS2 is the length of short axis 2, and Ll is the length of the long axis. The coagulation shape was determined by dividing the long axis length by the average length of the two short axes. A ratio near 1 indicates a more spherical shape of the heat-induced coagulation, whereas deviation from a ratio of 1 implies that the shape of the coagulation is changing to oval.

Statistical Analyses
The Shapiro-Wilk test was used to determine if data were distributed normally. This was the case for all variables except volumes and shape ratios. The logarithms of the volumes and shape ratios were compared instead of the volumes and shape ratios themselves. In this case, the geometric mean is presented instead of the arithmetic mean. Differences were considered significant if the P value was less than .05. Results are presented as the mean and 95% confidence interval (CI).

Separate data analyses were performed for the single electrode and the cluster electrode. The Dunnett test was used to compare the lengths of the axes and the logarithm of the volumes of coagulation acheived at different magnetic field strengths with the corresponding values of ablations performed outside the magnetic field. For the single electrode, possible changes in coagulation symmetry were examined by comparing differences for x1 minus x2 and for z1 minus z2 for ablation performed outside the magnetic field with the corresponding differences at 0.2 T, 1.5 T, and 3.0 T. The Dunnett test was used for these comparisons. The assumption of equal variances was tested with the Levene test. All statistical analyses were performed with statistical software (JMP IN 5.1; SAS Institute, Cary, NC).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
Single Electrode
Mean short axis x length, short axis z length, and shape ratio were 2.3 cm, 2.6 cm, and 1.55, respectively, outside the magnetic field; 2.4 cm, 2.4 cm, and 1.62, respectively, at 0.2 T; 2.5 cm, 2.6 cm, and 1.51, respectively, at 1.5 T; and 2.2 cm, 2.5 cm, and 1.62, respectively, at 3.0 T (Fig 5, Table 1).


Figure 5
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Figure 5: Graph shows coagulation volume achieved with the single electrode and the cluster electrodes outside the magnetic field and at different magnetic field strengths. Data points are geometric means; error bars indicate 95% CIs of six measurements.

 

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Table 1. Coagulation Dimensions Inside and Outside the Magnetic Field

 
The geometric mean of the ablation volumes acheived with the MR-compatible single electrode was 12.1 cm3 outside the magnetic field (95% CI: 10.4 cm3, 14.2 cm3), 11.0 cm3 at 0.2 T (95% CI: 9.7 cm3, 12.5 cm3), 13.1 cm3 at 1.5 T (95% CI: 11.7 cm3, 14.7 cm3), and 10.7 cm3 at 3.0 T (95% CI: 8.4 cm3, 13.6 cm3). Coagulation volume changes of more than 12% were not observed.

Analysis of coagulation symmetry showed no significant influence of the magnetic field (at any strength) on coagulation symmetry either outside or inside the magnetic field. When the influence of different field strengths was compared in detail (Table 2), coagulation volume was reduced by 10% and 12% at 0.2- and 3.0-T MR imaging, respectively, and enlarged by 8% at 1.5-T MR imaging.


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Table 2. Comparison of Coagulation Size Inside and Outside the Magnetic Field

 
Cluster Electrode
Mean short axis x length, short axis z length, and shape ratio were 3.9 cm, 3.9 cm, and 1.17, respectively, outside the magnetic field; 3.7 cm, 3.8 cm, and 1.20, respectively, at 0.2 T; 4.0 cm, 4.3 cm, and 1.08, respectively, at 1.5 T; and 3.8 cm, 3.8 cm, and 1.17, respectively, at 3.0 T (Fig 5, Table 1).

No significant difference between coagulation volumes achieved inside and those achieved outside the magnetic field was observed when either the cluster electrode or the single electrode was used.

When the cluster electrode was used, mean ablation volumes were 35.4 cm3 outside the magnetic field (95% CI: 32.3 cm3, 38.9 cm3), 32.5 cm3 at 0.2 T (95% CI: 29.0 cm3, 36.3 cm3), 39.5 cm3 at 1.5 T (95% CI: 35.3 cm3, 44.1 cm3), and 33.9 cm3 at 3.0 T (95% CI: 29.6 cm3, 38.9 cm3). When we compared the different field strengths, coagulation volume was reduced by 8% at 0.2 T and by 4% at 3.0 T. At 1.5 T, coagulation volume was enlarged by 11%. When we compared the axis lengths, one significant difference was detected (P = .026) in the z-axis length at a field strength of 1.5 T: A difference of 4 mm in the length of the short axis parallel to the magnetic field was detected. However, as in all other cases, no significant difference in coagulation volume was found (Table 2).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 
In clinical practice, RF ablation is being increasingly used for tumor therapy (16,17). However, several challenges subsist in the field of RF ablation: First, techniques to increase the volume of tissue destroyed in a single treatment session must be developed. This can be achieved by combining RF ablation with therapeutic modalities, such as chemoembolization or alcohol injection (18,19). Second, further efforts to better understand how to integrate thermal ablation techniques into overall patient care need to be made. Third, more suitable and accurate imaging examinations must be developed to enable better monitoring of RF ablation. MR guidance has been shown to offer outstanding imaging properties not only for RF ablation but also for tumor treatment (eg, cryotherapy) (20,21).

With its excellent soft-tissue contrast and the possibility of being used for multiplanar imaging, MR imaging offers the advantage of near-online monitoring of the RF ablation procedure. The ability to immediately obtain MR images during and after intervention while performing RF ablation may facilitate safe treatment for tumors larger than those currently recommended for treatment. Furthermore, in addition to conventional MR imaging, temperature monitoring with techniques such as proton-resonance frequency shift–based phase-difference imaging or the balanced steady-state free precession method can be performed (22,23), thereby providing additional information for heat-induced coagulation delineation (7). However, if RF ablation is performed with MR guidance, the potential influence of the strong static magnetic field on the extent of ablation due to ion deflection and the resulting effects of Hall resistance must be investigated to ensure safe and effective ablation of malignant lesions. Thus, the patient may remain positioned inside the MR imager during the RF energy application, and the RF applicator may be repositioned during the same RF ablation session according to the MR findings in cases of incomplete ablation of the malignant tissue.

Theoretically, effects of magnetic fields on mobile ions and subsequent alterations of the coagulation extent are expected. The exact mechanism of RF energy transfer is, as yet, not completely understood. RF absorption mechanisms in biologic tissue are described in the Radiofrequency Radiation Dosimetry Handbook (24). With a frequency of 104–108 Hz, the so-called ß dispersion effect is dominant (ie, in this domain, absorption is mostly due to biologic macromolecules—such as proteins and nucleic acids—and the presence of biologic cells, especially if they are charged or have an excitable membrane). Electrolytes play a substantial role in the field of microwaves only at frequencies of 109 Hz. This may explain why deviations of electrolyte pathways do not seem to affect coagulation size. In addition, the influence of thermally induced molecular movements could be as pronounced as possible effects of magnetic field strengths on mobile ions.

The experimental setup was chosen for several reasons: Immersing the liver in a conductive 0.9% NaCl solution closes the electric circuit between the active electrode and the grounding pad. Thus, human tissue properties and clinical situations are simulated. The grounding pad should be located at a clearly defined distance from but not in close proximity to the active electrode to enable assessment of the effects of the magnetic field on the current pathway. The direction of the electric current flow between the active electrode and the plane of the grounding pad was orientated perpendicular to the magnetic field B0 to create the maximum possible influence of the magnetic field.

In preliminary experiments, no changes in electrical parameters (ie, impedance, voltage, power output, and current) were detected. Even if the absolute value of the electrical resistance itself is not changed, it is quite conceivable that the distribution of the electrical resistance is changed inside the magnetic field, leading to changes in the coagulation geometry. Thus, we focused on macroscopic analysis of the heat-induced coagulation.

In contrast to the findings of a preliminary study (11) that showed reduced coagulation volume when RF ablation was performed with different RF devices inside the magnetic field of clinical MR imagers, no significant influence of the magnetic field strength on ablation outcome was detected in the present study, which was performed with internally cooled RF electrodes. Furthermore, by performing ablation at different field strengths with two different RF devices, no definite tendency—neither reduction nor enlargement of coagulation volume nor shape of coagulation inside the magnetic field—could be identified. The length of the axes did not differ significantly between the different field strengths or inside or outside the magnetic field. Only RF ablation performed with the cluster electrode inside a 1.5-T MR imager showed a significant difference (P = .026) in one short axis (parallel to the magnetic field) compared with ablations performed outside the magnetic field. This could have been due to the fact that the overall volume obtained with the cluster electrode was larger than the volume obtained with the single electrode (ie, the variations are more evident and easier to record). However, in this particular case, a difference of only 4 mm was detected. This difference is small (only a few millimeters) and does not represent a clinically relevant difference. In addition, the overall volumes of coagulation obtained with the cluster electrode at different magnetic field strengths did not differ from those of the control group.

A limitation of this study could be that we performed ablations in ex vivo conditions. Mechanisms of interaction between the MR field strength and the coagulation size could be partially different in in vivo conditions. Thus, in comparison with other ex vivo studies, the coagulation volumes in our study were relatively small. This can be explained by our specific experimental setup, which allowed considerable cooling effects because the liver was completely immersed in the NaCl solution. Nevertheless, since the aim of our study was to compare the extent of coagulation in similar settings, the absolute value of the volume was less important than the reproducibility itself.

MR imaging is based on both static and alternating magnetic fields. Since no images may be routinely obtained during the RF ablation procedure itself (ie, during energy output from the generator), high-frequency alternating fields from excitation pulses and from gradient switching of the imager were not considered in this study.

One interesting point that was not investigated in this study is that MR electric interference may influence the electric fields surrounding the electrodes.

Further studies must be performed with bipolar RF devices, and the difference between outcomes when the neutral electrode is closer to the active electrode (thus limiting the area in which the MR device can alter the electric field of the RF generator) must be assessed.

Practical application: Although the exact mechanisms of RF energy absorption and the possible influence of magnetic fields at the molecular level is not yet clear, our findings show that RF ablation is not impaired by the static magnetic field of different clinical MR imagers. These findings have an essential effect on the global debates that will involve image-guided tumor ablation. MR guidance, which has the advantages of excellent soft-tissue contrast and near-online monitoring of heat-induced coagulation necrosis, may be used for RF ablation without the drawbacks of reduced coagulation volume or unfavorable coagulation shape. However, further tests with other RF applicators, such as an expandable electrode or a bipolar system, must be performed to complete the investigations in the field of MR-guided RF ablation.


    ADVANCE IN KNOWLEDGE
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 


    FOOTNOTES
 

Abbreviations: CI = confidence interval • RF = radiofrequency

See Materials and Methods for pertinent disclosures.

Author contributions: Guarantors of integrity of entire study, C.S., H.G., F.S., P.L.P.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, C.S., C.A., H.G., A.B., S.C., D.S., F.S., C.D.C., P.L.P.; experimental studies, C.S., C.A., H.G., A.B., S.C., D.S., F.S.; statistical analysis, T.H.; and manuscript editing, all authors


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCE IN KNOWLEDGE
 References
 

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RADIOLOGY RADIOGRAPHICS RSNA JOURNALS ONLINE