Infrahepatic inferior vena cava clamping with Pringle maneuvers for laparoscopic extracapsular enucleation of giant liver hemangiomas

From January 2012 to January 2016, 36 patients with giant liver hemangiomas underwent laparoscopic liver resection at Tongji Hospital of Huazhong University of Science and Technology, Wuhan, China. All of the procedures were performed by the same surgeon. This study was approved by the Ethics Committee for Clinical Pharmacology in Tongji Medical College. Giant liver hemangiomas were defined by a diameter larger than 10 cm. Based on the maneuvers of hepatic vascular occlusion, these patients were classified into two groups: IVC clamping and Pringle maneuver (IVCP group, n = 15) and Pringle maneuvers alone (Pringle group, n = 21) with laparoscopic extracapsular enucleation. Baseline data were similar between the two groups. Patients with hemangiomas that were adjacent to the main portal pedicle, major hepatic veins, or IVC were enrolled in this study. Patient’s clinical records were reviewed, including characteristics of liver hemangiomas, laboratory tests, surgical approaches, intraoperative variables, postoperative complications and mortality, and hospital stay days.

Surgical intervention, principally including liver anatomical resection and tumor enucleation, is the definitively curative treatment for liver hemangiomas. Recent advances in surgical techniques and established perioperative management have made liver resection or enucleation safe in most specialized units. When surgery is indicated, extracapsular enucleation is advocated by most surgeons. This surgical option can retain the maximum amount of normal liver parenchyma, minimize intraoperative blood loss, and decrease the incidence of postoperative biliary fistula in open surgery. However, with some liver hemangiomas, the distress caused by open surgery may be far worse than the tumor-related discomfort. Therefore, we prefer the laparoscopic approach for the treatment of hemangiomas.

With the progress of minimally invasive techniques, laparoscopic surgery for hepatic procedures has been rapidly developing. More complicated laparoscopic liver resections are now possible, including right hepatectomies, left hepatectomies, and even extended right and left hepatectomies [16, 17]. Compared with open surgical resection, laparoscopic resection offers many advantages, such as a shorter hospital stay, improved cosmetic results, and potential improvements to immunological outcomes [18, 19]. In order to reduce bleeding, in previous studies, laparoscopic anatomical liver resection was used for the removal of hepatic hemangiomas, but the procedure tends to result in excessive loss of liver tissues or even gallbladder [20]. In our study, 36 cases of liver hemangiomas were adjacent to the main portal pedicle, major hepatic veins, or gallbladder that previously recommended anatomical liver resection in laparoscopic hepatectomy. Nevertheless, we performed enucleation for all of the cases of liver hemangiomas. Enucleation has retained as much as possible of liver tissue, while giant hepatic hemangioma often close to the hepatic vein or portal vein leads to excessive bleeding especially for laparoscopic hepatic hemangioma enucleation and even results in the conversion to open surgery. Therefore, the hepatic vascular occlusion for bleeding control is critical to hepatectomy [21]. The Pringle maneuver could minimize hepatic arterial and portal blood flow to liver during transection of hepatic parenchyma; actually, a major cause of blood loss during liver resection is often attributed to the injury of hepatic vein [22]. Compared with bleeding from the portal vein and hepatic artery, hemorrhage from the injured hepatic vein is much more difficult to control throughout the whole laparoscopic hepatectomy procedure.

To decrease bleeding from the hepatic vein, low CVP which is controlled by anesthesiological methods has gained wide acceptance among hepatobiliary surgeons, based on the results of various randomized studies in the field of liver surgery [23, 24]. However, this finding has been contradicted by some other studies in which CVP monitoring did not appear to reduce blood loss in elective liver resection and globally, the intraoperative clinical value of CVP was questioned [25]. Rahbari et al. and our studies showed that infrahepatic clamping of the IVC significantly reduced intraoperative blood loss compared with anesthesiological methods of low CVP and that it did not reveal a significant association between the CVP and intraoperative blood loss irrespective of the applied method of reduction of CVP [15, 26]. In addition, infrahepatic IVC clamping may considerably reduce the adverse effects of reduction of CVP by anesthesiological interventions and the risk of intraoperative bleeding primarily from the hepatic veins [27, 28]. In this study, using IVC clamping to control blood loss, we were in a position to precisely identify the major vascular architecture around the hemangioma and selectively clip or ligate it, thus limiting blood loss during liver transection [14]. With fewer blood vessels traversing the capsule, the tumor can be enucleated without much blood loss by cutting open this layer between the capsule of the hemangioma and the liver. In our experience, the dissection of infrahepatic IVC is not so difficult and can be completed within a relatively short time (7–21 min). In the current study, we confirmed the advantages of infrahepatic IVC clamping to reduce blood loss under laparoscopic hepatectomies. Patients in the IVCP group experienced less blood loss and fewer blood transfusion requirements than those in the Pringle group. The total amount of blood loss in the IVCP group was significantly less than that in the Pringle group, and no patient in IVCP group had more than 1000 mL of blood loss during the operation.

Safety of portal triad clamping during liver resection has not been a matter of debate. IVC clamping technique with the Pringle maneuver has been thought to increase hemodynamic instability and postoperatively elevate the serum level of alanine aminotransferase, which can be deleterious in major liver resection in a diseased liver. In most cases, clamping IVC technique was well tolerated. The IVC was encircled at a site proximal to the bilateral renal veins; there was the potential risk of renal function impairment due to venous blood congestion [29]. However, there were no significant differences in intraoperative urine volume, postoperative BUN, and creatinine values between the groups. Furthermore, all of the liver function profile, such as AST, ALT, and TBil, did not fluctuate substantially and returned to normal ranges within a short period of time after operation. The risk of laparoscopic hepatectomy is CO₂ gas embolism (gas embolism), which is associated with pneumoperitoneum gas influx into the IVC or hepatic vein during liver parenchymal transection [30, 31]. Our experience showed that the enucleation of hepatic hemangioma mostly did not expose the inferior vena cava and short hepatic veins and their injury was comparatively less likely. The hepatic vein perhaps may encounter a small amount of carbon dioxide influx into the blood, but generally, this will not lead to an embolism. As the operation is carried out in a blood loss surgical field, we can easily clamp or control the bleeding from the hepatic vein with infrahepatic IVC clamping. To date, we have performed 36 patients with hepatic hemangioma surgery under laparoscopic resection with IVC clamping and Pringle maneuver. So far, we have performed roughly 80 such operations without any serious complications. In future, we will conduct further studies in this regard.

Our study had limitations. Intraoperative blood loss according to the type of clamping procedures was not assessed, because of the retrospective nature of this study. Therefore, it was unable to demonstrate any superiority of one clamping procedure upon another.

Infrahepatic clamping of the IVC and the Pringle maneuver significantly reduces intraoperative blood loss compared with the Pringle maneuver alone. IVC clamping and the Pringle maneuver may serve as a safe, effective, and feasible technique for enucleation of hepatic hemangioma.