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1 All authors: Department of Radiology, David Geffen School of Medicine at UCLA, BL-428 CHS/Box 951721, Los Angeles, CA 90095-1721.
Received October 30, 2003;
accepted after revision January 21, 2004.
Address correspondence to S. S. Raman
(sraman{at}mednet.ucla.edu).
Abstract
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MATERIALS AND METHODS. In seven pigs under anesthesia, a 17-gauge percutaneous insufflation needle was inserted in the infraumbilical midline using a standard insufflator. Three to six liters of CO2 was infused into the peritoneal space to achieve at least a 1-cm separation between the liver and the diaphragm and maintained by a pressure of 8–10 mm Hg. Seven control lesions in six historical controls were used. In addition, five lesions were created in one animal from this cohort who served as a control. Superficial areas of liver separated from diaphragm were fluoroscopically targeted for radiofrequency ablation, and several 2-cm-diameter radiofrequency lesions were generated. The pigs were sacrificed at 48 hr, and at laparotomy, the liver surface was inspected and sectioned to select lesions with centers within 1 cm of the surface. The thermal injury to the corresponding adjacent diaphragm was examined to determine the depth of injury. Diaphragmatic injury was graded on a scale from 0 to III (0, no injury; I, mild injury to one-third thickness; II, moderate injury to two-thirds thickness; III, severe injury to full thickness.)
RESULTS. Of 72 total lesions created, 60 had centers less than 1 cm from the liver surface (i.e., superficial) at laparotomy. Of these 60 lesions, 55 caused no significant diaphragmatic injury, two caused grade I injury and three caused grade III injury. In comparison, seven of seven historic superficial control lesions and five of five superficial radiofrequency control lesions from the current cohort caused grade III injury. Superficial radiofrequency lesions created after intraperitoneal CO2 insufflation caused significantly less (p < 0.01) diaphragmatic injury.
CONCLUSION. We have shown that in pigs, intraperitoneal CO2 insufflation helped significantly reduce severe diaphragmatic injury when superficial hepatic radiofrequency ablation was performed.
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Targeted carbon dioxide (CO2) insufflation has been used to manipulate intraperitoneal and retroperitoneal structures to provide a safer route for percutaneous procedures [10]. In a previous report [12], we described a saline infusion technique to help manipulate portions of the liver away from the diaphragm and reduce the incidence of thermal diaphragmatic injury during adjacent hepatic radiofrequency ablation. In this study we investigated whether percutaneous intraperitoneal insufflation with CO2 during subcapsular hepatic radiofrequency ablation would help minimize or eliminate diaphragmatic injury in a porcine model.
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The pigs were placed in the supine position after adequate anesthesia was achieved, and the right upper quadrant and epigastrium were shaved and surface-sterilized. Both thighs were shaved, and grounding pads were placed bilaterally.
In each animal from the experimental cohort, a 17-gauge insufflation needle (Endopath endosurgical, Ethicon) (Fig. 1) was then placed in the peritoneal cavity 2–3 cm below the umbilicus through a small incision. The insufflation needle was then connected to a CO2 insufflation apparatus (High Flow Insufflator, Stryker Endoscopy) used in the operating room for routine laparoscopy-assisted surgery. The settings were adjusted to provide a steady flow of CO2 at 0.1 mL/min to distend the abdomen and achieve a steady-state intraperitoneal pressure of 10 mm Hg for the duration of the procedure. Higher pressures theoretically may depress venous return. A total of 6–8 L of CO2 was delivered during the course of the procedure. A staff veterinarian helped monitor the animal by clinically assessing parameters such as jaw tone and monitoring heart rate, blood pressure, and blood oxygen saturation.
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A 15-gauge radiofrequency probe (LeVeen needle electrode, Boston Scientific) was used. This needle electrode is equipped with eight retractable, curved distal hooks (or tines) which, when fully expanded, assume an umbrella shape 2 cm in maximum diameter perpendicular to the axis of the probe. In a previous report [8], we showed that percutaneous radiofrequency ablation resulting in thermal lesions at the liver surface (center of lesion < 1 cm from capsule) caused significant injury in the adjacent apposed diaphragm.
We used fluoroscopy to help guide the creation of a number of superficial liver lesions expediently and assess the feasibility of the CO2 insufflation technique. In our dedicated animal laboratory, fluoroscopic guidance (Angiostar, Philips Medical Systems) helped easily localize the liver silhouette in the right upper quadrant before and after CO2 insufflation. The probe was advanced to the hepatic parenchyma, and the expandable tines were deployed. A 90-W monopolar radiofrequency generator (RF 2000, Radiotherapeutics) was used as the energy source. Power output was initially set at 30 W and titrated manually to maintain maximal power without rise in impedance for at least 5 min. After rapid impedance rise, power output automatically terminated, and after 1 min a second cycle was initiated at 80% of maximal power.
Using fluoroscopic guidance, we were able to directly visualize liver separation from the diaphragm. Viscera were easily identified fluoroscopically and avoided. The stomach was easily identified because of characteristic internal contents and placement of a nasogastric tube. The small bowel and colon were easily identified because of internal gas and characteristic location. To evaluate the efficacy of the CO2 insufflation technique in attenuating or eliminating diaphragmatic injuries, we attempted to create peripheral subcapsular, nearly spherical lesions of 2 cm in diameter (2-cm LeVeen radial diameter) with centers approximately 1 cm from the liver surface. The LeVeen needle electrode was placed approximately 1 cm deep relative to the liver capsule, and the tines were expanded to create a 2-cm-diameter radiofrequency lesion. A total of 72 lesions were created in the seven experimental animals using the equipment and parameters discussed.
The pigs were sacrificed immediately, and a postmortem examination was performed. The liver and diaphragmatic surfaces adjacent to the thermal subcapsular hepatic lesions were inspected and photographed (Fig. 2). The harvested liver was sectioned, and all superficial thermal lesions were measured and tabulated (Fig. 3). The diaphragm was resected and sectioned. On the basis of previous experience, thermal diaphragmatic injury was easily recognized visually as a round or ovoid firm, tan area adjacent to thermal liver lesions. Representative gross cross sections of diaphragmatic injuries were taken to determine the degree of injury. Diaphragmatic thermal injuries on cross sections were graded on a scale of 0–III (0, no diaphragmatic injury; I, mild injury up to one-third thickness; II, moderate injury to two-thirds thickness; and III, severe injury to full thickness) (Fig. 4). This grading system applied best to the muscular central diaphragm, which permitted ease of visual estimation of injury grade.
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Because this study was a variation of a previously published study [11], the control group consisted of two subgroups: historic controls and current controls. In the historic subgroup, we used seven lesions from the control group (six animals) of our prior study because all other factors (animal breed, animal weight, radiofrequency equipment, and radiofrequency technique) were similar. In the current control subgroup, five separate subcapsular radiofrequency thermal lesions were created before intraperitoneal CO2 insufflation in a single animal. The control group (historic and current subgroups) was compared against the post-CO2 insufflation group with respect to the extent of diaphragmatic injury. The significance of differences in values was determined using Barnard's test of proportions [13].
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All 12 control lesions in seven animals produced liver surface injury and adjacent transdiaphragmatic injury (grade III), including seven of seven lesions in the historic subgroup and five of five lesions in the current control subgroup. After intraperitoneal CO2 insufflation, a total of 72 experimental lesions in seven animals were created (Table 1). Of the 72 lesions, 60 were superficial on postmortem examination and liver sectioning. All 12 deeper lesions produced no diaphragmatic injury. Of the 60 superficial lesions, 55 produced no significant adjacent diaphragmatic injury. Of the remainder, two of five lesions produced grade I diaphragmatic injury (less than one-third thickness) and three lesions produced grade III diaphragmatic injury. These lesions were all located in the high diaphragmatic dome, near the bare area (three lesions) or at the extreme right lateral margin of the liver (two lesions). Using Barnard's test of proportions, superficial thermal lesions created after intraperitoneal CO2 insufflation caused significantly less overall diaphragmatic injury when compared to both current and historic controls.
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In this study, we applied a commonly used laparoscopic surgical technique to assist percutaneous manipulation of the anterior and dome portions of the diaphragm. Previously, we described a saline infusion method to isolate the liver to minimize or eliminate concurrent diaphragmatic injury in an in vivo porcine model when the liver surface was injured during thermal ablation [8]. In this study performed in a similar in vivo porcine model, we have shown the feasibility of using intraabdominal CO2 insufflation to help isolate portions of the liver from the adjacent diaphragm, decreasing the rate of diaphragmatic injury without clinically significant complications related to CO2 insufflation. The use of CO2 has been previously described in the radiology literature to help manipulate retroperitoneal structures for percutaneous access. However, to our knowledge, the current application has not been described. Advantages of CO2 over saline infusion include more rapid distention of the peritoneal cavity and therefore separation of the diaphragm from the liver, as well as other heat-sensitive structures such as bowel, without the need for large quantities of fluid administration. CO2 can be rapidly absorbed by the peritoneum and excreted in the lungs. It can also be aspirated to quickly relieve complications related to depressed venous return resulting from excessive intraabdominal distention and pressure. Gas, unlike fluid, is also a natural insulator that conducts heat more readily. CO2 has been widely used for laparoscopic radiofrequency ablation and, indeed, one of the perceived advantages of laparoscopic over percutaneous radiofrequency ablation is that surface lesions are more easily treated without damaging the adjacent diaphragm or organs. Therefore, this advantage of laparoscopic radiofrequency ablation can be offered through a percutaneous technique, without using operating room time, the laparoscope, or laparoscopic sonography. The difference is that CT or CT fluoroscopy would be required for imaging guidance. Although an increased risk of bleeding has been described during percutaneous liver biopsy when the liver is separated from the diaphragm and abdominal wall [14, 15], these concerns are likely minimized with radiofrequency ablation because of its inherently coagulative nature. In our study, no significant hemorrhagic complications related to lack of tamponade of the liver surface were reported.
Limitations of this study include the applicability of data from a porcine model to humans. This study was conducted with one radiofrequency device, and conclusions may not necessarily apply to others. Also, no histologic sections of grossly normal diaphragm were taken. The visual grading system applies best to the muscular central diaphragm, because it is thickest. Thermal injuries to the thin peripheral diaphragm tend to produce full-thickness injuries. We did not test arterial blood gas in pigs for potential acidosis. However, abdominal CO2 insufflation is routinely performed in both humans and animals for a variety of laparoscopic procedures. This technique, if applied to humans, will require conventional CT or CT fluoroscopic guidance. Sonographic guidance may have a limited role. Finally, the extent of visible lesions on the liver surface was estimated and not quantified.
In summary, we have developed a percutaneous method to manipulate and separate the liver from the diaphragm in a pig model. We have also shown that percutaneous CO2 insufflation may help limit the magnitude of diaphragmatic injury when radiofrequency ablation is performed on superficial, subcapsular lesions adjacent to the diaphragm. Further refinements to this technique are necessary to adapt it for human use.
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