TECHNICAL REPORT

New Technique of Extracorporeal Hepatic Inflow Control for Pure Laparoscopic Liver Resection Toru Mizuguchi, MD, PhD,* Masaki Kawamoto, MD, PhD,* Yukio Nakamura, MD, PhD,* Makoto Meguro, MD, PhD,* Thomas T. Hui, MD, FACS,w and Koichi Hirata, MD, PhD*

Abstract: We have developed a new technique of the Pringle maneuver by clamping outside the abdominal wall for pure laparoscopic liver resection (pure Lap). Our technique successfully controls bleeding and enables pure Lap to be completed without any events, even for a large tumor. Between 2008 and 2010, we compared consecutive patients who received pure Lap with (n = 11) and without (n = 7) this Pringle maneuver. Although tumor size in the Pringle group was significantly larger than in the no-Pringle group (3.35 ± 1.64 vs. 1.11 ± 0.29 cm, respectively), intraoperative bleeding was not significantly different (165.5 ± 188.5 vs. 177.9 ± 364.4 mL, respectively). In contrast, operation time in the Pringle group was significantly longer than in the noPringle group (343.1 ± 99.5 vs. 199.6 ± 63.2 min, respectively). Pure Lap for large tumors is feasible when employing a new Pringle maneuver outside the abdominal wall. Key Words: hepatic inflow vascular control, liver resection, pure laparoscopic surgery

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aparoscopic liver resection (Lap) was first reported in 1991 as an incidental treatment for benign liver tumors during gynecologic laparoscopic surgery.1 Since then, a pure laparoscopic approach2–4 and hand-assisted approach5–7 for Lap have been developed.8,9 The greatest obstacle to applying pure Lap for every single liver resection is bleeding from Glisson pedicles and hepatic veins. Unlike the open procedure, to control bleeding in pure Lap is very difficult unless some procedures for controlling hepatic inflow or outflow is employed before bleeding.10,11 Bleeding from hepatic veins can be controlled to increase pneumoperitoneal pressure or decrease central vein pressure.12,13 However, it is still difficult to control bleeding from the Glisson pedicle without vascular control during pure Lap. Various techniques have been used for vascular clamping of the hepatoduodenal ligament (known as the Pringle maneuver) during pure Lap.14,15 We have developed a new technique for control of hepatic inflow by clamping outside the abdominal wall. Our technique successfully controls bleeding during the pure Lap procedure and makes Received for publication May 13, 2013; accepted July 11, 2013. From the *Department of Surgery I, Sapporo Medical University Hospital, Sapporo Medical University, Sapporo, Hokkaido, Japan; and wDepartment of Surgery, Children’s Hospital & Research Center Oakland, Oakland, CA. Supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (No. 23591993) and a grant from the Yuasa Memorial Foundation. The authors declare no conflicts of interest. Reprints: Toru Mizuguchi, MD, PhD, Department of Surgery I, Sapporo Medical University School of Medicine, S-1, W-16, Chuo-Ku, Sapporo, Hokkaido 060-8543, Japan (e-mail: [email protected]). Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved.

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it possible to conduct the entire procedure without any events, even for large tumors. Herein, we report preliminary clinical results of pure Lap using hepatic inflow control from outside the abdominal wall in comparison with the classical pure Lap approach without hepatic inflow control.

PATIENTS AND METHODS Patients In January 2008, a prospective study of pure Laps for hepatocellular carcinoma was initiated. All the patients should be grade A in Child-Pugh classification without distant metastasis or vascular invasion. The laparoscopic approach was considered on the basis of the size and location of the tumor. We started with a tumor size within 2 cm, located on the liver surface, and at least 3 cm from the inferior vena cava without a Pringle maneuver (no-Pringle group: n = 7). In January 2009, we enlarged the indication to a tumor size within 10 cm and at least 3 cm from the vena cava because of the development of a hepatic inflow control technique (Pringle group: n = 11).

Surgical Technique The study was approved by the institutional review board and all procedures were performed after obtaining informed consent from all participating individuals. The patient position was right lateral decubitus for tumors in the right lobe and supine with open legs for tumors in the left lobe. The first trocar was placed exactly at the umbilicus and CO2 gas was insufflated into the peritoneal cavity at 8 to 10 mm Hg after exploratory intra-abdominal examination. Five trocars were used for the pure LAP approach without vascular control and 6 trocars were used for the pure LAP approach with hepatic inflow control, the so-called Pringle maneuver. The trocars were located in a radial manner and the umbilical trocar was at the center. The liver cutting line was 2 cm away from the tumor edge and was precoagulated with a microwave coagulater (Microtaze; Alfresa Pharma Inc., Osaka, Japan), Biclamp (ERBE Elektromedizin GmbH, Tu+bingen, Germany), and EndoSH 2.0 (Salient Surgical Technologies, Portsmouth, NH). A cavitron ultrasonic aspirator (CUSA Excel; Integra LifeSciences Co., Plainsboro, NJ) was used for dissection of the liver parenchyma. Basically, a 2-surgeon technique was used. The operator used a CUSA with a retracter and the assistant used the coagulator with a retracter. The umbilical trocar was used for the Pringle maneuver after insertion of the other 5 trocars. An intermittent Pringle maneuver was applied with 10-minutes warm ischemia and 5-minutes reperfusion when bleeding was seen at the dissecting plane. Preoperative blood chemical tests, operative variables, and tumor characteristics were recorded whenever it was necessary.

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FIGURE 1. Pringle kit consisting of 40 cm silicon tube, 10 mm in diameter, and 100 cm of polyester tape, 5 mm wide, from outside the abdominal wall for pure laparoscopic liver resection (A). The hepatoduodenal ligament is encircled using a snake-shaped retractor and tied to the polyester tape (B). The tape is extracted through the umbilical port and penetrates the silicon tube (C). Thereafter, the silicon tube is slid into the abdominal wall along with the tape and clamp, using a Pean clamp to prevent air leakage (D).

Extracorporeal Pringle Maneuver Method Hepatic inflow control method of the extracorporeal procedure is shown in Figure 1. We used a 40 cm silicone tube, 10 mm in diameter, and a 100 cm long polyester tape, 5 mm wide (Fig. 1A). After encircling the hepatoduodenal

ligament with the polyester tape by using a snake-shaped retractor (Fig. 1B), the edge of the tape was pulled out through the umbilical trocar and the silicon tube was inserted (Fig. 1C). The tape and tubes were clamped with a Pean clamp to prevent air leakage and slipping (Fig. 1D).

FIGURE 2. A 78-year-old man who had hepatocellular carcinoma in the posterior segment with a tumor 7 cm in diameter. Preoperative axial computed tomography scan (A) and 3-dimensional computed reconstruction image (B). Trocar scars at 4 weeks after surgery (C). Postoperative axial computed tomography scan (D) and 3-dimensional computed reconstruction image (E). The size of the specimen including the tumor was 14 10 cm (F). Arrow pointing at the right hepatic vein.

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FIGURE 3. A 70-year-old woman who had hepatocellular carcinoma in the anterior segment with a tumor 5.5 cm in diameter. Preoperative axial computed tomography scan (A) and 3-dimensional computed reconstruction image (B). Trocar scars at 4 weeks after surgery (C). Postoperative axial computed tomography scan (D) and 3-dimensional computed reconstruction image (E). The size of the specimen including the tumor was 7 6 cm (F). Arrows pointing at the middle hepatic veins.

Statistical Analysis Continuous data were analyzed using the one-way analysis of variance. The differences between the groups for categorical data were compared using the w2 test followed by a post hoc 2 2 Fisher exact test, when needed. The calculations were performed using the StatView 5.0 software package (Abacus Concepts Inc., Berkeley, CA) or SPSS 16.0 (SPSS Inc., Chicago, IL).

RESULTS We developed a new method for hepatic inflow control from outside the abdominal wall through a trocar. Although this method requires an additional trocar site for hepatic vascular inflow control, it is very easy and safe for pure Lap. Representative cases using extracorporeal Pringle maneuver are shown in Figure 2 for a posterior segment tumor and in Figure 3 for an anterior segment tumor. The posterior tumor was 7 cm in longitudinal diameter (Figs. 2A, B). The tumor was taken out through the extent umbilical trocar site and a few scars were recognized after surgery (Fig. 2C). Postoperative computed tomography revealed that the anatomic posterior segment was nearly removed and the right hepatic vein was exposed on the edge of the cutting surface (Figs. 2D, E). The size of the specimen was 14 10 cm (Fig. 2F). The anterior tumor was 5.5 cm in diameter (Figs. 3A, B). Pure laparoscopic splenectomy was completed 3 weeks before liver resection because of hypersplenism with severe thrombocytosis. The spleen and the liver specimens were

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taken out through the umbilical trocar site and the patient was satisfied with postabdominal scar (Fig. 3C). Postoperative computed tomography revealed that the anatomic anterior subsegment was removed and the middle hepatic vein was exposed on the edge of the cutting surface (Figs. 3D, E). The size of the specimen was 7 6 cm (Fig. 3F). Overall clinical demographics are shown in Table 1. No 90-day mortality was recorded and all complications were within grade III according to the Clavien Classification of Surgical Complications. Although 1 case in the no-Pringle group was converted into open surgery because of massive bleeding from the right hepatic vein, no conversion was needed in the Pringle group. The patients in the Pringle group were significantly older than those in the noPringle group (67.5 ± 7.6 vs. 51.3 ± 10.2 y, respectively). Although tumor size in the Pringle group was significantly larger than that in the no-Pringle group (3.35 ± 1.64 vs. 1.11 ± 0.29 cm, respectively), intraoperative bleeding was not significantly different (165.5 ± 188.5 vs. 177.9 ± 364.4 mL, respectively). In contrast, operation time in the Pringle group was significantly longer than that in the no-Pringle group (343.1 ± 99.5 vs. 199.6 ± 63.2 min, respectively).

DISCUSSION We developed a new method for the Pringle maneuver from outside the abdominal wall during pure Lap. Even though pure Lap was conducted for larger tumors, operative safety regarding morbidity and mortality was secured. Despite the longer operative time, pure Lap was feasible for

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TABLE 1. Clinical Demographics of Pure Laparoscopic Liver Resection With and Without the Pringle Maneuver Method

Clinical Variables Sex (M:F) Etiology B:BC:C:NBNC:AL Age (y) Albumin (g/dL) Bilirubin (mg/dL) PT (%) Platelets ( 104/mm3) AST (IU/L) ALT (IU/L) ICG R15 (%) Prealbumin (ng/mL) Tumor sizes (cm) Operation time (min) Bleeding (mL) Blood transfusion (U) Blood transfusion (Y:N) Complication (Y:N)

No-Pringle Group (n = 7)

Pringle Group (n = 11)

2:5

4:7

5:0:0:2:0 51.3 ± 10.2 3.92 ± 0.45 0.96 ± 0.82 88.96 ± 11.28 13.12 ± 4.29 29.1 ± 17.4 25.1 ± 18.8 18.33 ± 19.09 23.43 ± 2.67 1.11 ± 0.29 (0.7-1.5) 199.6 ± 63.2 177.9 ± 364.4 0.57 ± 1.51 1:6 2:5

4:1:3:1:2 67.5 ± 7.6 3.81 ± 0.27 0.75 ± 0.47 94.01 ± 8.97 15.28 ± 5.69 35.6 ± 14.9 34.6 ± 19.2 10.17 ± 3.93 18.66 ± 6.36 3.35 ± 1.64 (1.0-7.0) 343.1 ± 99.5 165.5 ± 188.5 0.36 ± 1.21 1:10 4:7

P 0.732 0.211 0.002 0.545 0.513 0.351 0.465 0.446 0.366 0.203 0.239 0.003 0.004 0.751 0.751 0.503 0.732

ALT indicates alanine aminotransferase; AST, aspartate aminotransferase; AL, alcoholic hepatitis; B, HBV hepatitis; BC, HBV and HCV hepatitis; C, HCV hepatitis; NBNC, non-B non-C hepatitis; ICG R15, indocyanine green retention rate at 15 minutes; PT, prothrombin time.

large tumors as long as the new Pringle maneuver outside the abdominal wall was employed. Hepatic inflow control, known as the Pringle maneuver, can reduce massive bleeding during the liver resection.13,16 Although the clinical value of the Pringle maneuver is still controversial in the open procedure,17 it seems to be the only way to control bleeding from the Glisson pedicle. Unlike in the open procedure, it is very difficult to control bleeding by compression of the liver parenchyma during pure Lap.11,15,18,19 The Pringle maneuver has already been reported to be necessary for the pure Lap.11,18 In fact, several methods for the Pringle maneuver have been reported for the pure Lap approach.14,15,18 The originality of our method is the use of a long tube with a wide clamp tape. The route of the long tube can be located at the most dorsal position compared with the other working routes, including the laparoscopy route. Therefore, our Pringle maneuver does not interfere with working manipulations or while visualizing the entire operating field. As far as the wide tape is concerned, there were 2 patients who developed portal thrombosis after open liver resection using a 3 mm polyester tape for the Pringle maneuver. Although portal thrombosis might be associated with poor liver function,20 it is most likely because of vascular injury caused by the Pringle maneuver.21 Therefore, we believe that wide tape is needed to avoid this complication, and no portal thrombosis was recorded after we began to use it in this series. One of the concerns for the Pringle maneuver is bleeding during unclamping.16 Recent hemostatic devices can reduce bleeding during liver resection and nicely seal the bile duct as well.22 The sealing effect can be enhanced under hepatic inflow control during liver resection because the cooling effect of the blood flow is reduced. Therefore, bleeding from the cut surface was minimal even during reperfusion. Even though the anatomic segmental mass was not removed totally, the anatomic surgical margin can be secured, as we have shown in the results. In contrast, unexpected liver functional mass could be lost in this Copyright

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procedure. We should be careful not to excessively ablate the liver parenchyma, and the heating effect can be enhanced under hepatic inflow control. In conclusion, we developed a new method for hepatic inflow control from outside the abdominal wall for pure Lap. Pure Lap for large tumors is feasible when applying this method. The exact indication for pure Lap should be determined in the future. ACKNOWLEDGMENTS The authors thank Kim Barrymore and Sandy Tan for their help in preparing this manuscript and for their valuable discussion. REFERENCES 1. Reich H, McGlynn F, DeCaprio J, et al. Laparoscopic excision of benign liver lesions. Obstet Gynecol. 1991;78:956–958. 2. Dulucq JL, Wintringer P, Stabilini C, et al. Laparoscopic liver resections: a single center experience. Surg Endosc. 2005; 19:886–891. 3. Vibert E, Perniceni T, Levard H, et al. Laparoscopic liver resection. Br J Surg. 2006;93:67–72. 4. Sasaki A, Nitta H, Otsuka K, et al. Ten-year experience of totally laparoscopic liver resection in a single institution. Br J Surg. 2009;96:274–279. 5. Fong Y, Jarnagin W, Conlon KC, et al. Hand-assisted laparoscopic liver resection: lessons from an initial experience. Arch Surg. 2000;135:854–859. 6. Cuschieri A. Laparoscopic hand-assisted hepatic surgery. Semin Laparosc Surg. 2001;8:104–113. 7. Kitaoka F, Yanaga K, Okudaira S, et al. Successful left adrenalectomy for metastatic hepatocellular carcinoma using hand-assisted laparoscopic surgery: report of a case. Surg Today. 2005;35:172–174. 8. Koffron A, Geller D, Gamblin TC, et al. Laparoscopic liver surgery: shifting the management of liver tumors. Hepatology. 2006;44:1694–1700. 9. Nguyen KT, Geller DA. Is laparoscopic liver resection safe and comparable to open liver resection for hepatocellular carcinoma? Ann Surg Oncol. 2009;16:1765–1767.

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10. Huscher CG, Lirici MM, Chiodini S. Laparoscopic liver resections. Semin Laparosc Surg. 1998;5:204–210. 11. Cherqui D, Husson E, Hammoud R, et al. Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg. 2000; 232:753–762. 12. Uchiyama K, Ueno M, Ozawa S, et al. Half clamping of the infrahepatic inferior vena cava reduces bleeding during a hepatectomy by decreasing the central venous pressure. Langenbecks Arch Surg. 2009;394:243–247. 13. Chouillard EK, Gumbs AA, Cherqui D. Vascular clamping in liver surgery: physiology, indications and techniques. Ann Surg Innov Res. 2010;4:2. 14. Maehara S, Adachi E, Shimada M, et al. Clinical usefulness of biliary scope for Pringle’s maneuver in laparoscopic hepatectomy. J Am Coll Surg. 2007;205:816–818. 15. Cho A, Yamamoto H, Nagata M, et al. Safe and feasible inflow occlusion in laparoscopic liver resection. Surg Endosc. 2009;23:906–908. 16. Smyrniotis V, Farantos C, Kostopanagiotou G, et al. Vascular control during hepatectomy: review of methods and results. World J Surg. 2005;29:1384–1396.

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17. Lee KF, Wong J, Ng W, et al. Feasibility of liver resection without the use of the routine Pringle manoeuver: an analysis of 248 consecutive cases. HPB (Oxford). 2009;11: 332–338. 18. Descottes B, Lachachi F, Sodji M, et al. Early experience with laparoscopic approach for solid liver tumors: initial 16 cases. Ann Surg. 2000;232:641–645. 19. Zhen ZJ, Lau WY, Wang FJ, et al. Laparoscopic liver resection for hepatocellular carcinoma in the left liver: Pringle maneuver versus tourniquet method. World J Surg. 2010;34:314–319. 20. Targarona EM. Portal vein thrombosis after laparoscopic splenectomy: the size of the risk. Surg Innov. 2008;15:266–270. 21. Shen P, Fleming S, Westcott C, et al. Laparoscopic radiofrequency ablation of the liver in proximity to major vasculature: effect of the Pringle maneuver. J Surg Oncol. 2003;83:36–41. 22. Mizuguchi T, Katsuramaki T, Nagayama M, et al. Rapid recovery of postoperative liver function after major hepatectomy using saline-linked electric cautery. Hepatogastroenterology. 2008;55:2188–2192.

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New technique of extracorporeal hepatic inflow control for pure laparoscopic liver resection.

We have developed a new technique of the Pringle maneuver by clamping outside the abdominal wall for pure laparoscopic liver resection (pure Lap). Our...
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