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Experimental Studies |
1 From the Department of Diagnostic Radiology (P.L.P., J.T., I.S., C.T.R., D.S., C.D.S.), Section of Experimental Radiology (J.B.), and Departments of General Surgery (M.S.), Forensic Medicine (J.S.), and Pathology (S.K.), Eberhard-Karls-University, Hoppe-Seyler-Strasse 3, 72076 Tübingen, Germany. From the 2002 RSNA scientific assembly. Received February 13, 2003; revision requested May 1; final revision received October 31; accepted January 2, 2004. Address correspondence to P.L.P. (e-mail: philippe.pereira@med.uni-tuebingen.de).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Four commercially available RF devices (perfusion, internally cooled cluster, and nine- and 12-tine expandable electrodes) that represent the most widely used systems on the market were tested. Sixteen in vivo ablation procedures were performed in porcine livers (four ablations for each RF system). After macroscopic and histopathologic analyses of 3-mm-thick liver sections, morphometric and volumetric findings in the central zone of white coagulation necrosis were assessed. Coagulation volume, diameter, length, and shape were determined digitally. After analysis of variance, measurements with each system were tested with the Tukey post hoc test.
RESULTS: Mean coagulation volumes were 31.5 cm3 ± 15.8 (SD) for the perfusion electrode, 20.5 cm3 ± 2.6 for the cluster electrode, 16.2 cm3 ± 7.3 for the 12-tine electrode, and 9.8 cm3 ± 3.2 for the nine-tine electrode (P < .05, perfusion vs nine-tine electrode). No significant differences were observed regarding the mean short axis perpendicular to the needle shaft: 2.30 cm ± 0.94, 3.04 cm ± 0.26, 3.44 cm ± 0.21, and 2.70 cm ± 0.76, respectively. Variation coefficients were 0.50, 0.13, 0.45, and 0.33, respectively.
CONCLUSION: Larger coagulation volumes were obtained with the perfusion and internally cooled cluster devices. More spherical volumes of ablation were achieved with the 12-tine and cluster electrodes. The former proved superior with regard to the short axis perpendicular to the needle shaft. The cluster and nine-tine electrode produced better reproducibility, which is suggestive of improved predictability of the extent of coagulation with these systems.
© RSNA, 2004
Index terms: Animals • Experimental study, 761.1269 • Liver, interventional procedures, 761.1269 • Radiofrequency (RF) ablation, 761.1269
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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One challenge for successful thermal ablation of solid tumors is to ensure induction of coagulation of the entire targeted volume with as few applications as possible. Thus, a major limitation remains the maximum volume of coagulation that can be achieved in one RF session. Since the description of RF ablation for liver therapy in 1990 (3), quickly growing interest in this technique may be attributed to the introduction of RF devices with the major aim of enhancing the amount of local energy deposition. These devices haveenabled the creation of larger ablation zones, with more recent acceptance of RF ablation to treat large tumors in many solid organs, including the liver, bones, kidneys, lungs, thyroid, and breasts (4–10).
Especially for the liver, multiple strategies have been attempted to improve the effectiveness of thermal ablation techniques. On one hand, these improvements have resulted from clinical modifications with either combined strategies with local injections (11,12) or methods for reduced blood flow (13–16). On the other hand, technical developments with electrode designs (17–20), optimized ablation algorithms (21,22), more powerful generators (23), or even bipolar techniques (19) have been beneficial. Thus far, however, the greatest improvements in RF outcome are mostly attributable to better understanding of the biophysical principles and performance of the procedure, as well as to modifications of RF systems.
Current commercially available electrodes are configured as perfusion or internally cooled straight electrodes, parallel clustered internally cooled straight electrodes, or multitined expandable electrodes. If each of these techniques is aimed to increase the extent of coagulation with different apparatuses or ablation algorithms, local tissue heating remains the mechanism that underlies their effectiveness.
The purpose of our study was to compare in vivo coagulation necrosis obtained with four RF ablation devices, to determine shape and reproducibility of induced coagulation by means of three-dimensional measurements of the ablation zone, and to achieve representations of the coagulated areas in three-dimensional spaces.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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For the RF ablation procedures, animals were placed in the supine position. The following anesthetics were injected intramuscularly: 20 mg per kilogram of body weight of ketamine hydrochloride (Clorketam; Vetoquinol, Lure, France), 4 mg/kg azoperone (Stressnil; Janssen-Cilag, Issy-les-Moulineaux, France), and 0.05 mg/kg atropine sulfate (Aguettant, Lyon, France). After cannulation of an auricular vein, sodium pentobarbital (Pentobarbital Sodique; Sanofi, Libourne, France) was administered intravenously in a bolus dose (6 mg/kg) to facilitate endotracheal intubation. Ringer lactate solution (Sanofi) was continuously infused during the experiment (300 mL/h). Anesthesia was maintained with isoflurane in oxygen (0.3 L/min) by using a respirator (15 breaths per minute, positive pressure of 20 cm H2O). Cardiac and respiratory parameters were monitored throughout the entire observation time. After the right jugular vein had been surgically isolated, a 3-F catheter (Endocath; Plastimed, St Leu-la-Foret, France) was placed in the superior vena cava. The upper area of the right abdomen and the epigastrium were shaved and sterilized. A Mercedes abdominal incision was made to expose the complete liver.
The animals were euthanized 2 hours after the last RF ablation procedure with a pentobarbital (Dolethal; Vetoquinol) overdose of 60 mg/kg. The livers were then removed and fixed in 10% neutral buffered formaldehyde solution.
Study Design
All experiments and histopathologic examinations were performed between December 2001 and June 2002. For the four RF systems tested, all parameters and generator settings were determined in strict accordance with the manufacturer’s guidelines. Technical data for the RF devices are shown in Table 1. Only one ablation session was performed, according to the algorithms developed and tested by the manufacturers. According to these algorithms, two ablation phases are achieved with the HiTT 106 and RF 3000 systems. All procedures were performed with continuous digital recording in real time with the device interfaces for the Cool Tip and model 1500 systems (D.S., J.B.). The HiTT 106 system accumulates energy during the procedure and displays the electric data. Total ablation time was also computed from the stored ablation data.
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RF Devices, Ablation Protocols, and Settings
HiTT 106.—This perfusion RF system is a 375-kHz generator capable of producing a maximum power of 60 W through a 1.7-mm-diameter monopolar electrode with an active needle tip length of 1.5 cm (24). The electrode for this saline-enhanced technique is double walled at its distal part, while the inner wall has small holes. The infused isotonic saline solution flows through the hollow shaft of the electrode and permeates through the holes into the space between the inner and outer walls of the needle tip (Fig 1a). The outer wall is constructed with large rectangular apertures that permit fluids to be injected into the tissue that surrounds the needle tip before and after the ablation procedure. Continuous interstitial perfusion of sterile saline was started 30 seconds (rate, 20 mL/h) prior to energy application. Uniform saline infusion was achieved with a digitally controlled syringe pump (Pilot C; Fresenius Vial, Brezins, France). RF current was applied for 20 minutes with a power of 40 W, in accordance with the manufacturer’s recommendations. One grounding pad was attached to the animal’s flank.
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above the baseline value. At this point, the current is switched off automatically to avoid further local increase in temperature, which would result in tissue charring. Fifteen seconds later, the current automatically switches on again, thus generating the pulsed RF technique that increases the size of RF ablation areas (21).
RF 3000.—This RF system makes use of a multitined monopolar expandable electrode connected to a 480-kHz generator capable of producing a maximum power of 200 W. The 2.5-mm-diameter cannula of the electrode (LeVeen; Radiotherapeutics) contains 12 retracted curved distal tines, which when fully expanded form an umbrella shape, 4 cm in maximum diameter, perpendicular to the axis of the probe (Fig 1c). After deployment of the tines, power output was initially set at 80 W and then increased in 10-W increments every 30 seconds to 130 W. With no increase in impedance over 200 after 5 minutes at 130 W, power output was increased in 10-W increments every 30 seconds to 190 W and maintained until either 15 minutes of application time had elapsed or an uncontrolled impedance rise was observed. After 30 seconds, a second phase was started, and RF energy was applied until the next uncontrolled impedance rise occurred. In case of an uncontrolled impedance rise in the first 5 minutes at an initial power of 130 W, power was reapplied after 30 seconds with 50% of the power at which the impedance rose. Subsequent power output was increased in 10-W increments every 30 seconds to 190 W and maintained until either 15 minutes total application time had elapsed or until the next impedance rise. Two such applications, without change in probe position, were used to create each ablation area with this system (23,25). Four grounding pads were attached for each procedure, as recommended by the manufacturer.
Model 1500.—In this RF system, the expandable electrode consists of an insulated outer needle with a diameter of 2.2 mm that houses nine deployable curved tines (Starburst XL; Rita Medical Systems). When the electrodes are fully extended, the maximum diameter is 5 cm and mimics the configuration of a Christmas tree (Fig 1d). Five of the tines contain a thermocouple in the tips that allow temperature recording during the ablation procedure. Alternating electric current proceeds from a 150-W generator operating at 460 kHz. Electrodes were progressively extended deeper into the liver parenchyma, with temperature monitoring, to represent the standard algorithm widely used with this system. The standard method allows the maximum energy to be applied until the mean temperature reaches the threshold. Tines were first deployed at 2 cm with a preselected target temperature of 80°C, then advanced to 3 cm with a targeted temperature of 105°C, and finally extended to 4–5 cm with a targeted temperature of 110°C. The targeted temperature had to be maintained for 7 minutes prior to monitoring of postablation temperatures with the five thermocouples. For this system, two grounding pads were placed on the thighs (23).
Histopathologic Study and Three-dimensional Evaluations
After extirpation, all livers were preserved in neutral buffered 10% formaldehyde for 3–4 weeks. Attention was paid to provide appropriate extirpation, preparation, and storage of the livers to avoid deformations in the recipients. The livers were then embedded in gelatin and serially sectioned at exactly 3-mm intervals approximately perpendicular to the probe shafts. Four guide marks had been implanted in the liver parenchyma to prevent further deformations of the ablated area as a result of the manipulations. These guide marks were also necessary to perform optimal three-dimensional analyses and imaging.
For histopathologic analysis, the extent of ablated volume was determined macroscopically on each 3-mm section at gross pathologic examination and at microscopy after hematoxylin-eosin staining. Each region of interest was excised and examined by a pathologist (S.K.) to strictly differentiate between the central "white zone" of complete coagulation and the peripheral "red zone" of hyperemia, since the hyperemic zone may be variable and does not automatically reflect definite coagulation. This differentiation was possible in all cases. Pathologic examinations were performed without knowledge of the specific RF device used. In addition, DNA strand breaks were examined (M.S.) by means of immunohistochemical assay (Tunel; Boehringer, Mannheim, Germany), which was performed according to the manufacturer’s instructions. For all comparative measurements, only central white coagulation was assessed (Fig 2) because it represents the zone in which complete cellular destruction is assured (26).
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To assess the short axis of the ablation zone, defined as the maximum diameter perpendicular to the electrode shaft, the extent of coagulation was measured for each thermally induced lesion in three representative central slices: two maximal transverse diameters perpendicular to the electrode shaft (d1 and d2) were measured at three contiguous sections, and the average was calculated. The coagulation length l was obtained in the needle axis by adding the number of 3-mm-thick sections with induced coagulation from the top to the bottom of each thermally induced lesion (taking into account only the central white coagulation) and multiplying by 3 to obtain the maximum length. The shape S was then defined by dividing l by the average of d1 and d2. Thus, a ratio near 1 emphasizes a more spherical shape of the thermally induced lesion. A value of S > 1 implies oval coagulation with the longer diameter parallel to the electrode shaft, whereas a value of S < 1 implies oval coagulation with longer diameter perpendicular to the electrode shaft. In addition, we calculated a coefficient of variability of the volume of coagulation as a measure for reproducibility. The closer the value is to 0, the more reproducible the coagulation.
Statistical Analyses
Coagulation volumes, diameters, lengths, and shapes were digitally recorded and are reported as the mean ± SD for all dimensions. To stabilize variances in groups, data were log transformed before analysis of variance was performed with the fixed factor "device" (four levels) and the random factor "pig." Estimates were obtained with the restricted maximum likelihood method (JMP, version 5.0.1.2; SAS Institute, Cary, NC). For direct comparison of two samples, the Tukey post hoc test was used. Differences with a value of 
< .05 were considered to be statistically significant.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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The largest mean volumes of coagulation were produced with both perfused electrodes (ie, the HiTT 106 [31.5 cm3 ± 16.8] and Cool Tip [20.5 cm3 ± 2.6] electrodes, respectively) connected to a 60- or 250-W generator, with mean ablation times of 19.5 minutes ± 1.0 and 12.1 minutes ± 1.2. The multitined expandable RF 3000 12-tine and the model 1500 nine-tine electrodes, respectively, produced volumes of 16.2 cm3 ± 7.3 and 9.8 cm3 ± 3.2, with mean ablation times of 13.8 minutes ± 6.9 and 20.5 minutes ± 2.4. A significant difference in coagulation volume was observed between the HiTT 106 and model 1500 electrodes with a 150-W generator (P < .05). Differences were not significant between the perfused electrodes or between the multitined expandable electrodes.
Overall, comparison of the lengths of the ablation zone in the plane of the needle axis showed a significant difference between the HiTT 106 perfusion system and the multitined systems (perfusion electrode vs 12-tine electrode, P = .002; perfusion electrode vs nine-tine electrode, P = .02). The mean length of the coagulated area was 5.85 cm ± 1.50 for the perfusion electrode compared with 3.10 cm ± 0.62 for the 12-tine electrode and 3.83 cm ± 0.38 for the nine-tine electrode. Thus, maximum length did not correspond to the volume of coagulation. On the basis of findings in the present study, results with the four devices were in the following descending order: HiTT 106, Cool Tip, model 1500, and RF 3000.
Geometry of Coagulated Area
The most spherical ablated areas were produced with the RF 3000 electrode, with a calculated shape value of S = 0.90 (ratio of length to shortest axis). The longest dimension was parallel to the electrode axis for both perfused electrodes and for the nine-tine electrode and was perpendicular to the needle axis for the 12-tine electrode. Therefore, the thermally induced lesions obtained near the cluster electrode with S = 1.38 were slightly more ellipsoid in the plane of the electrode shaft. The nine-tine electrode produced a slightly more inverted conical shape (S = 1.42). The calculated shape with the HiTT 106 electrode can only be approximated (S = 2.54) because of the large irregularities of all coagulated areas induced with this system (Fig 4a). Thermally induced lesions obtained with this device were more cylindric along the needle shaft. Therefore, because of the irregular shapes obtained with this system, only the measurements of length and short axis can be considered reliable and representative. The coefficients of variability were significantly different (P < .05) with the HiTT 106 and Cool Tip electrodes at 0.50 and 0.13, respectively. Deformations of the coagulation shape were observed when a large vessel was close to the RF delivery area, regardless of which system was used (Fig 4b). The three-dimensional virtual images confirmed the two-dimensional measurements of coagulation geometry (Fig 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Regarding the saline perfusion electrodes, the ongoing diffusion of the heated fluid is also responsible for the ablation effect, in addition to static thermal conduction of the RF energy with subsequent local heating. The tissue conductivity is improved by infusing saline that contains electrically conductive ions. Indeed, the larger volumes of coagulation obtained with this device are probably the final result of the effects of heated fluid with better thermal conductivity (29) combined with continuous infusion of saline, which extends the conductive surface area of the electrode through a higher local ionic concentration (30). In a previous study (24), the amount of saline injected during ablation varied between 38 and 120 mL/h, which influenced the impedance of the tissue that underlay the ablation area. A disadvantage in that ex vivo experiment, however, was the uncontrolled diffusion of the boiling saline into the tissue, which led to irregular shapes of induced coagulation.
Finally, considering the power differences between the four generators used in this study, it becomes evident that the power output is not of primary importance with an electrode with open perfusion. However, a certain balance exists between the amount of energy deposited and the tissue heating; excessive power output leads to overheating and tissue desiccation. No further enlargement of diameters of RF-induced lesions was observed ex vivo for power between 30 and 60 W applied for 60 minutes with perfusion electrodes (24). One explanation could be that boiling frequently occurs at the electrode-tissue interface when power output is more than 50 W (30).
Since ablation of a tumor requires that the entire tumor and a margin of grossly normal tissue is encompassed by an ablation sphere, we consider that the shape of the induced coagulation area is at least as important as the coagulation volume. In clinical practice, the coagulation shape is determined by the configuration of the RF electrode, location of the tumor, tumor consistency, and perfusion-mediated cooling effect, as well as the saline distribution for open-perfusion devices. Findings in the present study confirm that ablation form is highly dependent on the type of RF system used. We achieved a more spherical ablated area with the 12-tine electrode, followed by the cluster electrode. This more spherical shape is explained by the umbrella geometry of the expandable electrode. The cluster electrode, which produces a larger coagulation area than does the 12-tine electrode, approximates a more ellipsoid shape in the coronal plane. The cluster electrode is composed of three straight probes arranged together and spaced 5 mm apart and has been proved to produce a nearly circular cross-sectional area of coagulation (28). The nine-tine electrode generates a thermal lesion that is somewhat conical (inverted), with deformations that correspond to the more peripheral localized prongs. In contrast, saline ablation produces the largest coagulation volumes, but the diffusion of fluid leads to marked distortions in the coagulation form. Creation of large but complex asymmetric coagulation shapes alone does not reflect the real effect of the device because the large volumes of coagulation did not automatically imply a large radius.
Livraghi et al (11) previously described the limitations of such irregularities of the coagulated area in clinical practice. The irregular pattern is related to uneven diffusion of heated fluids that results in inhomogeneous tissue impedance. Since liver tumors and especially liver metastases have heterogeneous consistency, the conductive saline will likewise follow preferential pathways through the impedances of the heterogeneous tumor tissue. Hence, more dense areas of tumor tissue may be partially unaffected by heat, and residual vital tumor cells may remain. On the other hand, the phenomenon of continuous saline diffusion could be advantageous in the treatment of encapsulated hepatomas because diffusion of hot saline could spread to the boundaries of the tumor. To date, experience with the HiTT 106 system for the treatment of hepatomas is encouraging but still limited (31). Further clinical investigations are needed.
Distortions of thermal lesion shape with uncontrollable extension of heat, as we observed (adjacent stomach was burned during ablation in the median area of the left liver lobe) with the HiTT 106 system may induce thermal damage in adjacent structures. Along these lines, Boehm et al (32) report a higher complication rate with saline-enhanced techniques in a comparison of internally cooled and perfusion electrodes for the treatment of breast cancers in an animal model.
Along with size and shape of the RF-induced lesion, reproducibility of the extent of coagulation is of primary importance for rigorous clinical application to assist the planning of ablation. In our experimental in vivo study with healthy porcine livers, coagulation volumes obtained with the cluster electrode were markedly more reproducible than were those induced with all the other electrodes. One explanation could be that the multitine electrodes are more sensitive to the surrounding tissue properties, especially regarding the heat-sink effect. If one or more prongs are located in a vessel, there is an irregular temperature or impedance profile, with subsequently greater variation in the ablation method. In a statistical analysis of their results, De Baere et al (27) found no significant difference in variability between a four-tine expandable electrode and a cluster electrode when ablation procedures were performed in vivo. On the other hand, reproducibility of saline-enhanced RF was shown by Livraghi et al (11) to be extremely low. Similarly, the RF-induced lesions we obtained with the perfusion electrodes may be considered unpredictable. Large irregularities in the ablation contours were observed when a large vessel was close to the RF delivery area, regardless of which RF system was used. This phenomenon was reported previously (28); it is called the heat-sink effect, which is a result of perfusion-mediating tissue cooling (vascular flow). Hansen et al (33) showed that in vivo coagulation may be shaped by the presence of vessels larger than 3 mm in diameter in the vicinity of the ablation area.
Finally, we also paid attention to the handling of the RF devices. We interrupted ablation procedures twice with the perfusion electrode because of a generator uncontrolled impedance rise. Although the perfusion was eventless, tissue charring at the needle tip caused complete occlusion of the apertures. In clinical practice, such an event necessitates insertion of a new electrode and repositioning of the obstructed electrode. In one other case, retraction of a fully expanded nine-tine electrode was incomplete as a result of the presence of desiccated tissue around the central prong of the electrode despite repeated saline flushes. Generators were used in accordance with the manufacturer’s recommendations without particular issues. All electrodes were placed with US guidance, and the echogenic response was generally satisfactory for all electrodes used in this experiment.
The time required to obtain the volumes of coagulation with ablation performed according to the manufacturers’ recommendations varied in our study from approximately 12 minutes for the Cool Tip internally cooled electrode and the RF 3000 12-tine expandable electrode to nearly 20 minutes for the HiTT 106 perfusion electrode and the model 1500 nine-tine expandable electrode. Hence, duration of one ablative session may affect the decision to use one RF system rather than another.
Several limitations of this study must be addressed. First, because of the small sample size, interpretations should be limited. Second, differences among the results obtained with the four RF devices are valid in healthy livers. Since some data may imply that tumor tissue is more sensitive to heat damage than is normal tissue (34), we consider these findings relevant. Nevertheless, it is likely that results will vary with other tumor tissue types because several tumor- and tissue-specific factors may modify the amount and extent of energy deposition. Since the aim of this experimental study was to compare RF systems rather than to study overall effectiveness, however, we believe that this limitation is acceptable. Another limitation is that we did not perform repeated ablation procedures with, for example, the pull-back technique, which is widely used in clinical practice but remains time-consuming. It can be argued that if a comparative study is intended to be scientifically valid, it has to be based on principles that have been proved to be easily reproducible in previous experiments. In accordance with this principle, it seemed impossible to respect the manufacturer’s guideline to perform only one ablation session for each experiment; this decision limited the uncertain aspect of repetitive ablation procedures. Because disparities among the RF systems represent one of the numerous problematic challenges for RF users, the primary end point of this in vivo study was to compare the most widely used ablation systems in similar conditions by not only assessing diameters and then projecting the volumes of coagulation achieved but also by analyzing the ablated volumes with three-dimensional calculations and mapping of the geometry of thermally induced lesions.
Practical application: The largest coagulation volume of ablated tissue was obtained with the HiTT 106 perfusion electrode connected to a digitally controlled saline infusion system. The largest mean coagulation volume produced in the most reproducible manner with an acceptable shape, however, was achieved with the Cool Tip cluster electrode connected to a 250-W generator. The RF 3000 12-tine expandable electrode with the umbrella configuration produced more spherical thermal ablation areas at the expense of more reduced ablation volume. Knowledge of the advantages and disadvantages of each RF system should support more appropriate routine clinical applications. All systems tested in this study demonstrated a certain degree of clinical success, however, and the physician’s expertise and tumor biologic features remain key factors. This study represents a snapshot in time because further refinements and improvements of current techniques will increase the effectiveness and further expand the role of RF ablation. Furthermore, the technical aspect represents only one challenge to be dealt with in the complex world of thermal ablation. We must attempt to better understand combined modalities, such as drug infusion combined with perfusion RF systems or chemotherapy combined with RF ablation, or further development of bi- or multipolar techniques. The best combination in the field of RF ablation, if such a combination exists, has yet to be determined, while taking into account that individual expertise is required for each tumor and organ.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, P.L.P., J.T., M.S., C.D.C.; study concepts, P.L.P.; study design, P.L.P., J.T., M.S., J.B.; literature research, D.S., I.S., M.S., S.K.; experimental studies, P.L.P., J.T., M.S., D.S., J.B., I.S.; data acquisition and analysis/interpretation, P.L.P., M.S., J.S., S.K., I.S.; statistical analysis, M.S., I.S.; manuscript preparation, P.L.P.; manuscript definition of intellectual content, P.L.P., C.D.C.; manuscript editing, P.L.P., C.T.R., C.D.C.; manuscript revision/review, C.D.C., C.T.R.; manuscript final version approval, P.L.P., C.D.C., C.T.R.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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