Surg Endosc DOI 10.1007/s00464-015-4276-9
and Other Interventional Techniques
Intermittent Pringle maneuver versus continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection Yu Zhang1 • Hongji Yang1 • Xiaofan Deng1 • Yunfei Chen1 • Shikai Zhu1 Chen Kai1
•
Received: 12 February 2015 / Accepted: 8 May 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Despite accumulated experience and advancing techniques for laparoscopic hepatectomy, bleeding remains the major concern during parenchymal transection. The vascular inflow control technique is still important to decrease intraoperative blood loss. The objective of this study was to compare intermittent Pringle with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection. Methods Between January 2011 and January 2015, a total of 79 consecutive patients with tumors locating either in the right or in the left hemiliver were included into this retrospective study (45 in the Pringle group vs. 34 in the half-Pringle group). Preoperative clinical characteristics, intraoperative details, postoperative complications and outcomes of patients were compared. Results The two groups were well matched according to clinical characteristics, tumor features, types of liver resection and histopathology (P [ 0.05). The mean operative time (247.5 ± 61.3 vs. 221.4 ± 48.7 min, P = 0.0446), ischemic duration (62.8 ± 28.3 vs. 44.1 ± 20.5 min, P = 0.0017) and overall declamping time (21.2 ± 8.2 vs. 0.9 ± 1.9 min, P \ 0.05) were significantly longer in the Pringle group
Yu Zhang and Hongji Yang have contributed equally to this work. & Yu Zhang [email protected] & Hongji Yang [email protected] 1
The Third Department of Hepatobiliary Surgery, Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), Chinese Academy of Sciences, No. 32 West Second Section, First Ring Road, Chengdu 610072, Sichuan, People’s Republic of China
than in the half-Pringle group. The mean amount of intraoperative blood loss (568.2 ± 325.1 vs. 420.7 ± 307.2 mL, P = 0.0444) and transfusion (266.1 ± 123.4 vs. 203.2 ± 144.6 mL, P = 0.0406) were significantly greater in the Pringle group. The overall operative morbidity rate was significantly higher in the Pringle group (40 vs. 17.6 %, P = 0.0324). The Pringle group was associated with significantly higher alanine aminotransferase and aspartate transaminase levels on postoperative day (POD) 7 and lower albumin levels on PODs 1 and 3 (P \ 0.05). The C-reactive protein levels were significantly higher in the Pringle group than in the half-Pringle group on POD 1 (37.5 ± 21.4 vs. 28.2 ± 19.0 mg/L, P = 0.0484), POD 3 (114.0 ± 53.4 vs. 90.6 ± 47.9 mg/L, P = 0.0474) and POD 7 (54.9 ± 29.8 vs. 40.1 ± 26.4 mg/L, P = 0.0245). Conclusion Continuous hemihepatic vascular inflow occlusion using extra-glissonian approach offers the advantages of less operative time and blood loss, less injury and better recovery in laparoscopic liver resection. Keywords Extra-glissonian approach Laparoscopic liver resection Liver neoplasm Pringle maneuver Hemihepatic vascular inflow occlusion Despite accumulated experience and advancing techniques for laparoscopic hepatectomy [1–4], bleeding remains the major concern during parenchymal transection [5–7]. Excessive blood loss and the need for blood transfusions are predictors of poor outcome for both noncirrhotic and cirrhotic liver resections [8, 9]. The vascular inflow control technique is still important to decrease intraoperative blood loss [10–12]. Some randomized controlled trials have been carried out to evaluate the impact of Pringle maneuver (total vascular inflow occlusion) and intermittent [13, 14] or continuous [15] hemihepatic
123
Surg Endosc
vascular inflow occlusion in open liver resection. These trials showed that total vascular inflow occlusion could be performed, but ischemic reperfusion injuries could lead to higher postoperative morbidity. However, hemihepatic inflow occlusion could decrease the amount of liver parenchyma submitted to reperfusion damage and offer the advantage of reduced blood loss [13, 14]. Some studies have demonstrated that laparoscopic liver resection with the intermittent half-Pringle maneuver is feasible and safe [16] and that laparoscopic glissonian approach is gaining popularity because it may reduce the time of operation and avoids dangerous and tedious laparoscopic dissection of liver hilum [17, 18]. However, continuous half-Pringle maneuver in laparoscopic liver resection has been reported limitedly. Because of the more technical difficulty associated with bleeding control, hemostasis at the transection plane, hilar dissection, the risk of gas embolism and deeper regions of the liver, we feel that continuous hemihepatic inflow occlusion could be even more useful in the laparoscopic context, especially using extra-glissonian approach. To our knowledge, there has been almost no study to compare intermittent Pringle maneuver with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach (half-Pringle maneuver) in laparoscopic liver resection. The objective of this study was to compare intermittent Pringle with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection.
Materials and methods Patients Between January 2011 and January 2015, a total of consecutive 79 patients with tumors locating either in the right or in the left hemiliver were considered to be included into this study, who underwent laparoscopic hepatotomy at the Third Department of Hepatobiliary Surgery, Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), Chinese Academy of Sciences. Data on these patients were analyzed retrospectively from a prospective database. Of the total 79 laparoscopic liver resections, 45 cases were performed by intermittent Pringle maneuver (the Pringle group), and the other 34 cases were performed by continuous hemihepatic vascular inflow occlusion using extra-glissonian approach (the half-Pringle group). The indications for the two groups were determined based on the same criteria: (1) elective liver resection; (2) tumors that were located either in the right or in the left hemiliver; (3) no major vascular involvement, and no tumor close to or even infiltrating the liver hilum; (4) tumor
123
size B8 cm, and extent of partial hepatectomy was a hemihepatectomy or less; (5) no concomitant surgical procedures except cholecystectomy; and (6) well-compensated chronic liver disease (Child-Pugh class A or B) without signs of severe portal hypertension (esophageal varices B F2). The preoperative workup consisted of a specified protocol including blood examinations, chest X-ray, abdominal ultrasound and contrast computed tomography scan. In selected cases, we performed spirometry, esophagogastroduodenoscopy and angiomagnetic resonance imaging. Liver function was assessed by the Child-Pugh grading. Laboratory blood tests included hemoglobin (HGB), white blood cell (WBC), platelet (PLT), albumin (Alb), alanine aminotransferase (ALT), aspartate transaminase (AST), serum total bilirubin (TBIL), prothrombin time (PT), international normalized ration (INR), HBsAg, antibodies to hepatitis C, serum alpha-fetoprotein (AFP), carcinoembryonic antigen (CEA), carbohydrate antigen 19-9 (CA199) and C-reactive protein (CRP). All procedures were performed after informed consents were obtained. All operations were performed by the same surgical team. This study was approved by the ethical committee of the Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), and it followed the ethical guidelines of the 1975 Declaration of Helsinki. Surgical procedure After appropriate preoperative preparation, the patient was taken to the operating room for laparoscopic hepatotomy. The patients received general anesthesia. When tumors located in the right hemiliver, the patients were placed in the left semidecubitus position with the right side elevated approximately 30°. Generally, five ports were used. The first trocar (12 mm) was inserted at the right-upper umbilicus for placement of a 10-mm 30° laparoscope. Four other trocars were inserted at the subxiphoid position (5 mm), at 5 cm superior to the umbilicus on the midline (12 mm), at 5 cm below the costal margin on the right midclavicular line (12 mm) and 2 cm below the costal margin on the right axillary line (5 mm) (Fig. 1). When tumors located in the left hemiliver, the patients were placed in the right semidecubitus position with the left side elevated approximately 15°. Five ports were used. The first trocar (12 mm) was inserted at the left of umbilicus for placement of a 10-mm 30° laparoscope. Four other trocars were inserted at 5 cm right superior to the umbilicus, at 2 cm below the costal margin on either the right or the left midclavicular line (5 and 12 mm) and 2 cm below the costal margin on the right axillary line (5 mm) (Fig. 2). After placing all trocars successfully, the operating table was tilted slightly to the reverse Trendelenburg position.
Surg Endosc
Fig. 2 Port placement When tumors located in the left hemiliver
together with the sling could be clamped with a Pean clamp to prevent gas leakage and sling slipping and the internal rubber catheter could protect hepatoduodenal ligament from injury by the hard catheter. Tightening of the sling and clamping of rubber catheter on the external end would result in vascular inflow occlusion. Tightening or loosening of the sling would result in clamping or unclamping of the entire liver. Intermittent vascular occlusion was performed with cycles of 15/5 min of clamp and unclamp times. For hemihepatic vascular inflow occlusion, the hilar plate was lowered, similar to the open technique as described by Hepp and Couinaud [19], to expose the confluence of the right and left portal pedicles by lifting the segment 4b of the liver (quadrant lobe) upward and incising the Glisson’s capsule at its base. Without entering the liver substance, a space could be developed by bluntly dissecting between the liver substance and the hilar plate. Either the right or the left portal pedicle was isolated en bloc and was encircled with a tourniquet to enable performance of a half-Pringle maneuver (Figs. 4, 5). Similar to the Pringle maneuver, tightening or loosening of the tourniquet would result in clamping or unclamping of the corresponding hemiliver. Separate clamping of the accessory left hepatic artery was necessary when it was present for control of the vascular inflow to the left hemiliver. The hemihepatic vascular occlusion was continuous if the parenchymal transection time was not more than 60 min, or else 5 min of reperfusion was required, despite which occurred seldom. The half-Pringle maneuver resulted in a visible line of ischemic demarcation along the main liver fissure (Cantlie line) (Fig. 6). The parenchymal transection was performed using the ultrasonic dissector (Harmonic Scalpel; Ethicon EndoSurgery). Bipolar electrocoagulation was used for minor bleeding. Intraparenchymal control of the major vessels was obtained with titanium clips, vascular locks or suturing
Exploration of the abdominal cavity was performed routinely. Intraoperative ultrasound was performed to confirm the extension of the tumor, the number of lesions and their position in relation to the main hepatic structures. The area to be resected was marked by electrocautery. If necessary, cholecystectomy was carried out. For Pringle maneuver, the avascular lesser omentum was divided, and a sling was placed around the entire hepatoduodenal ligament and passed through a 16-Fr hard catheter for use as a tourniquet to enable performance of a Pringle maneuver. Both ends of the hard catheter were connected by a 2-cm soft rubber catheter. The internal end of the catheter was close to the pedicle and the external end was extracorporeal, allowing for easy external occlusion (Fig. 3). When clamping, the external rubber catheter
Fig. 3 Pringle maneuver
Fig. 1 Port placement When tumors located in the right hemiliver
123
Surg Endosc
using prolene sutures. Linear laparoscopic staplers (Echelon 60 ENDOPATH Stapler, Ethicon Endo-Surgery, LLC, Cincinnati, OH, USA) were used to transect the major vascular structures, including the left/right hepatic pedicle, left/right hepatic vein and inferior right hepatic vein. The central venous pressure was kept below 5 mmHg during liver parenchymal transection [5], and continuous carbon dioxide pneumoperitoneum pressure was induced at a pressure lower than 12 mmHg to reduce the risk of gas embolism. Postoperative management
Fig. 4 Right portal pedicle was isolated en bloc and encircled with a sling
All patients received the same postoperative care by the same team of surgeons. Postoperative parameters of hepatic damage and recovery, including serum TBIL, ALT, AST, Alb, creatinine, PT, INR and CRP, were measured on postoperative days (PODs) 1, 3 and 7. The abdominal ultrasound examination was repeated on POD 7. Statistical methods Results were expressed as mean ± standard deviation and were analyzed by paired-sample t (t0 ) test. And the v2 test (with continuity corrected v2 if the expected count was \5) or the Fisher exact test was appropriate for categorical data. All calculations were performed using the SPSS 17.0 statistical software. Results with P value \0.05 (paired-tailed test) were considered statistically significant.
Results Fig. 5 Left portal pedicle was isolated en bloc and encircled with a sling
Baseline characteristics and surgical feasibility The two groups were well matched according to clinical characteristics, tumor features, types of liver resection and histopathology (P [ 0.05). The preoperative clinical and laboratory parameters were comparable in both groups of patients (Table 1). The mean size of the tumors was 4.4 ± 2.3 cm in the Pringle group, which was comparable to that in the half-Pringle group (4.6 ± 2.5 cm) (P = 0.7134). There were no significant differences between the two groups in terms of types of liver resection performed, percentage of main tumor with satellite nodules and patients with portal hypertension (Table 1). The histopathology of tumor or nontumorous liver was comparable between the two groups of patients (Table 2). Intraoperative results
Fig. 6 Visible line of ischemic demarcation along the main liver fissure (Cantlie line)
123
All of the patients underwent R0 resection. There was no margin invasion in the both groups. The tumor-free resection margin was comparable between the two groups of patients. Of
Surg Endosc Table 1 Clinical characteristics of patients
Pringle (n = 45)
Half-Pringle (n = 34)
t (v2)
P value
0.0599
0.8067
Sex M
29
21
F
16
13
Age (years)
47.3 ± 11.4
49.8 ± 13.6
0.8879
0.3773
BMI
22.4 ± 4.2
23.2 ± 3.8
0.8729
0.3855
WBC count (109/L)
5.2 ± 2.5
4.8 ± 2.8
0.6686
0.5057
PLT count (109/L)
168.4 ± 66.4
186.9 ± 73.5
1.1709
0.2452
HGB (g/L)
112.3 ± 28.5
123.8 ± 31.4
1.6996
0.0932
Grade A, n
38
30
0.0236
0.8778
Grade B, n
Child-Pugh classification 7
4
ALT (U/L)
41.3 ± 27.8
46.0 ± 25.3
0.773
0.4419
AST (U/L)
34.9 ± 18.5
36.7 ± 19.3
0.4203
0.6754
TBIL (lmol/L)
15.4 ± 5.1
16.6 ± 4.3
1.1063
0.2720
Alb (g/L) INR
39.7 ± 4.4 1.06 ± 0.18
41.3 ± 5.1 1.08 ± 0.21
1.4941 0.455
0.1392 0.6504
Creatinine (lmol/L)
65.3 ± 17.6
67.5 ± 16.8
0.5609
0.5765
CRP (mg/L)
7.9 ± 6.7
7.4 ± 7.1
0.3201
0.7498
Tumor size (cm)
4.4 ± 2.3
4.6 ± 2.5
0.3686
0.7134
Main tumor with satellite nodules, n
3
2
0.1055
0.7453
Patients with portal hypertension, n
7
5
0.0109
0.9170
AST aspartate transaminase, ALT alanine aminotransferase, Alb albumin, TBIL serum total bilirubin, INR international normalized ration, HGB hemoglobin, WBC white blood cell, CRP C-reactive protein
the total 79 cases, three cases were converted from a laparoscopic to an open procedure due to uncontrollable bleeding. The percentage of conversions was comparable between the two groups of patients (P [ 0.05). The mean operative time (247.5 ± 61.3 vs. 221.4 ± 48.7 min, P = 0.0446), ischemic duration (62.8 ± 28.3 vs. 44.1 ± 20.5 min, P = 0.0017) and overall declamping time (21.2 ± 8.2 vs. 0.9 ± 1.9 min, P \ 0.05) in the Pringle group were significantly longer than those in the half-Pringle group. The mean amount of intraoperative blood loss in the Pringle group was significantly greater than that in the half-Pringle group (568.2 ± 325.1 vs. 420.7 ± 307.2 mL, P = 0.0444). As a result, there was a significantly greater volume of intraoperative blood transfusion in the Pringle group (266.1 ± 123.4 vs. 203.2 ± 144.6 mL, P = 0.0406). No differences were observed in the percentage of patients transfused and the volume of crystalloid administered (P [ 0.05). In the halfPringle group, the mean time taken to prepare the hemihepatic vascular inflow occlusion was 19.3 min (range 8–27 min), which decreased to \15 min (range 8–15 min) in the last 15 cases of half-Pringle procedures. Postoperative complications and outcomes In this study, both groups had no perioperative mortality, which was defined as death within 90 days of surgery or death during the same hospital admission of surgery. There
was no evidence of intraoperative or postoperative gas embolism in any of the patients. No bile duct injury occurred in either group. Postoperative hospital stay was similar in the two groups (P [ 0.05). Postoperative ascites was defined by an abdominal drainage output more than 500 mL/day, or required treatment to be controlled. Hepatic insufficiency was defined as a PT of more than 50 % of normal and/or by serum bilirubin of more than 50 lmol/L on POD 7 or thereafter and/or encephalopathy. There was no significant difference in any type of complications (P [ 0.05); however, the overall operative morbidity rate in the Pringle group was significantly higher than that in the half-Pringle group (40 vs. 17.6 %, P = 0.0324). More details are reported in Table 3. The liver functional status on PODs 1, 3 and 7 as reflected by the postoperative changes of albumin, serum bilirubin, transaminase levels and INR is shown in Table 3. ALT and AST levels in both groups increased dramatically following surgery. The mean ALT level on POD 1 was about 16 times and the mean AST level on POD 1 was about 17 times comparing to preoperative levels in the Pringle group. The mean ALT level on POD 1 was 12 times and the mean AST level on POD 1 was about 13 times comparing to preoperative levels in the half-Pringle group. No significant differences were observed in ALT and AST levels on PODs 1 and 3 between the two groups (P [ 0.05). On POD 7, the ALT and AST levels in
123
Surg Endosc Table 2 Intraoperative detail of patients t/t0 (v2)
P Value
1
0.0527
0.8184
5
0.0034
0.9536
Pringle (n = 45)
Half-Pringle (n = 34)
Segment III
3
Segment II ? III
8
Type of liver resection, n
Segment II ? III ? IV
4
4
0.0018
0.9658
Segment V
5
4
0.0713
0.7894
Segment VI
5
3
0.0018
0.9658
Segment VII
3
4
0.1519
0.6968
Segment V ? VI
6
4
0.0180
0.8933
Segment VI ? VII
2
2
0.0527
0.8184
Segment V ? VI ? VII
4
3
0.1519
0.6968
5
4
0.0713
0.7894
Hepatocellular carcinoma
22
19
0.3794
0.5379
Cholangiocarcinoma
4
2
0.0050
0.9437
Segment V ? VI ? VII ? VIII Pathologic diagnosis, n
Mixed hepatocholangiocarcinoma
2
1
0.0617
0.8039
Metastases of colorectal carcinoma
3
3
0.0050
0.9437
Hemangioma
10
8
0.0188
0.8909
Focal nodular hyperplasia
2
0
Stromal tumor
2
1
0.5034 0.0617
0.8039
Nontumorous liver, n Normal
20
13
0.3070
0.5795
Chronic hepatitis
6
5
0.0236
0.8778
Cirrhosis
19
16
0.1836
0.6683
38
29
0.0109
0.9170
0.0617 2.0421
0.8039 0.0446
Tumor-free resection margin [1 cm 0–1 cm Conversion to open liver resection, n Operation time(range) (min)
7
5
2 247.5 ± 61.3 (90–380)
1 221.4 ± 48.7 (80–335)
Ischemic duration (range) (min)
62.8 ± 28.3 (30–120)
44.1 ± 20.5 (26–80)
Overall declamping time(range) (min)
21.2 ± 8.2 (5–35)
0.9 ± 1.9 (0–5)
3.2587 16.0466
0.0017 \0.05
Intraoperative blood loss (mL)
568.2 ± 325.1
420.7 ± 307.2
2.0441
0.0444
Intraoperative blood transfusion (mL)
266.1 ± 123.4
203.2 ± 144.6
2.0828
0.0406
Patients transfused, n
11
7
0.1637
0.6858
2737 ± 1113
2556 ± 1035
0.7374
0.4631
Crystalloid perfused (mL)
both groups were restored to near normal; however, the Pringle group was associated with significantly higher ALT and AST levels than the half-Pringle group (P \ 0.05). The indication to use intravenous albumin was albumin level \25 g/L together with ascites or hepatic insufficiency after operation in this study. The percentage of patients supplemented with intravenous albumin was similar in the two groups (P [ 0.05). The Pringle group was also associated with significantly lower albumin levels on PODs 1 and 3 (P \ 0.05). There were no significant differences in the bilirubin and the creatinine levels between the two groups (P [ 0.05). Mean CRP concentrations were similar preoperatively (P [ 0.05), and there was an increase in the plasma concentration of CRP in both groups following surgery. The
123
mean CRP levels were significantly higher in the Pringle group than in the half-Pringle group on POD 1 (37.5 ± 21.4 vs. 28.2 ± 19.0 mg/L, P = 0.0484), POD 3 (114.0 ± 53.4 vs. 90.6 ± 47.9 mg/L, P = 0.0474) and POD 7 (54.9 ± 29.8 vs. 40.1 ± 26.4 mg/L, P = 0.0245).
Discussion Laparoscopic liver resection is safe and may provide improved patient outcomes when compared to the open technique [20–23]. Long-term results show that oncological benefits of a laparoscopic approach are similar to open surgery [23–25]. With the improvement in laparoscopic
Surg Endosc Table 3 Postoperative complications and outcomes
Pringle (n = 45)
Half-Pringle (n = 34)
t (v2)
P value
Postoperative complications Postoperative bleeding, n
1
0
1.0000
Hepatic insufficiency, n
2
0
0.5034
Surgical site infections, n
1
1
1.0000
Cardiac insufficiency, n
1
0
1.0000
Creatinine transient elevation
1
0
Bile leakage, n
2
1
0.0617
Pulmonary infection, n
2
1
0.0617
0.8039
Ascites, n
5
2
0.1680
0.6819
Pulmonary effusion, n
6
0.0713
0.7894
1.0000
3 a
b
0.8039
Operative morbidity, n (%)
18 (40.0 %)
6 (17.6 %)
4.5752
0.0324
Patients using intravenous albumin, n (%)
4
1
0.3701
0.5429
656.5 ± 487.3 601.3 ± 402.8
563.8 ± 378.5 490.3 ± 312.2
0.9189 1.332
0.3610 0.1868
Postoperative outcome POD 1 ALT (U/L) AST (U/L) TBIL (lmol/L)
15.3 ± 7.8
13.3 ± 8.3
1.0977
0.2757
Alb (g/L)
27.5 ± 3.8
29.3 ± 3.3
2.2039
0.0305
INR
1.10 ± 0.54
1.08 ± 0.61
0.1541
0.8779
Creatinine (lmol/L)
65.3 ± 17.6
67.5 ± 16.8
0.5609
0.5765
CRP(mg/L)
37.5 ± 21.4
28.2 ± 19.0
2.0057
0.0484
POD 3 ALT (U/L)
237.4 ± 156.7
218.9 ± 143.5
0.5385
0.5918
AST (U/L)
284.3 ± 177.8
265.1 ± 183.7
0.4685
0.6407
TBIL (lmol/L)
35.3 ± 9.8
33.6 ± 7.4
0.8452
0.4006
Alb(g/L)
31.4 ± 4.7
33.8 ± 5.2
2.1465
0.0350
INR
1.22 ± 0.62
1.20 ± 0.58
0.1459
0.8844
Creatinine (lmol/L)
55.4 ± 13.7
51.2 ± 15.6
1.2708
0.2076
CRP (mg/L)
114.0 ± 53.4
90.6 ± 47.9
2.0146
0.0474
ALT (U/L) AST (U/L)
67.7 ± 28.4 74.4 ± 34.6
54.3 ± 21.5 58.9 ± 26.7
2.2972 2.1684
0.0243 0.0332
TBIL (lmol/L)
18.4 ± 7.7
16.5 ± 8.2
1.056
0.2943
Alb (g/L)
31.8 ± 5.1
32.7 ± 4.6
0.8096
0.4206 0.7365
POD 7
INR
1.13 ± 0.55
1.0 9 ± 0.48
0.3378
Creatinine (lmol/L)
47.9 ± 17.8
45.5 ± 20.1
0.5612
0.5763
CRP(mg/L)
54.9 ± 29.8
40.1 ± 26.4
2.294
0.0245
8.8 ± 2.7
8.4 ± 2.3
0.694
0.4897
Postoperative hospital stay(days) a
Twenty-one complications occurred in 18 patients
b
Eight complications occurred in six patients
equipments [6, 7] and the accumulation of clinical experience in laparoscopic and hepatic surgery, the indications for laparoscopic liver resection are expanding, including the type of resection and the size or location of the tumor [26, 27]. Although many limitations have been overcome, bleeding is still the most important problem that hinders the development of laparoscopic liver resection. Surgeons still
face challenging resections that require specific and innovative maneuvers to decrease intraoperative blood loss, as bleeding together with subsequent blood transfusion increases postoperative morbidity and mortality and enhances tumor recurrence in patients undergoing hepatectomy for liver malignancy [8, 9]. Pringle maneuver is the traditional and the most commonly used method to decrease blood loss during hepatic
123
Surg Endosc
parenchymal transection because of its effectiveness and simplicity, but can be associated with prolonged ischemic time. Laurent et al. [28] reported that laparoscopic liver resections are associated with higher ischemic times. Fu et al. [13] reported that both Pringle and half-Pringle maneuvers were safe and efficacious in reducing blood loss. Patients subjected to intermittent hemihepatic vascular inflow occlusion responded better than those with Pringle maneuver in terms of earlier recovery of postoperative liver function. And Ni et al.’s study [14] confirmed that in patients with HCC with cirrhosis, intermittent hemihepatic vascular inflow occlusion was still a better inflow occlusion method than Pringle maneuver. Liang et al. [15] reported a prospective randomized trial to compare continuous hemihepatic with intermittent total hepatic inflow occlusion in open hepatectomy. Liang et al. [15] suggest that continuous hemihepatic inflow occlusion is safe and effective, similar to intermittent total hepatic inflow occlusion, and it is recommended for complex liver resection. The above-mentioned studies were all carried out to compare the impact of Pringle maneuver with hemihepatic vascular inflow occlusion in open liver resections. [13–15]. Chen et al. [16] have reported half-Pringle maneuver using extra-glissonian approach in laparoscopic liver resections. However, intermittent half-Pringle maneuver was performed in his study (15/5 min), instead of continuous half-Pringle maneuver. To the best of our knowledge, our study is the first specific series to compare intermittent Pringle with continuous hemihepatic inflow occlusion using extra-glissonian approach in laparoscopic liver resections. Previous experience in more simple laparoscopic hepatic resections is necessary to any laparoscopic complex liver resection. Similarly, we consider indispensable previous experience with the extra-glissonian approach in open surgery. It is evident that no attempt should be made without experience performing open extra-glissonian approach. But if meeting these two requirements, the technique is surprisingly simple and effective. The procedure of hemihepatic inflow occlusion using extra-glissonian approach in laparoscopic liver resections required experience of the surgeon. Once the surgeon had acquired the technique, the preparation of the hemihepatic vascular inflow occlusion could be accomplished in about 15 min. It took\15 min (range 8–15 min) in the last 15 cases of halfPringle procedures in our study. Once the portal pedicles were exposed, either the left or the right portal pedicle could be encircled with a sling. Tightening or loosening of the sling would result in clamping or unclamping of the corresponding hemiliver. The procedure using extra-glissonian approach without entering the liver substance can be performed easily and rapidly, with minimal bleeding by blunt maneuvers without hilar dissection, and is better than
123
separate isolation of the hepatic artery, duct and portal vein [29]. The extra-glissonian approach allows safe en masse control of the portal structures without prolonged dissection, since it is exceptional (in 1 % of case) to have any vascular interposition between the inferior surface of the liver and the hilar plate [30]. We did not encounter any difficulties or excessive bleeding during preparation of the hemihepatic vascular inflow occlusion in this study. The extra-glissonian approach has been proven useful in open hepatectomies [31], which has also been used in different laparoscopic surgical procedures [16–18]. The advantages of this approach may be enhanced in the laparoscopic context. Tranchart [32] reported that in the patients that underwent laparoscopic liver resection for malignancy, operative time was the sole independent predictor of postoperative morbidity. Postoperative complication rate increases by 60 % with each additional operative hour during laparoscopic liver resection [32]. The mean operative time was significantly longer in the Pringle group than in the halfPringle group, which could be caused by the longer ischemic duration and overall time in declamping periods in the Pringle group. Another important reason was that surgeons had to spend more time controlling bleeding in the Pringle group. The amount of blood loss in the declamping periods was great, because it is very difficult to perform total compression of a wide transection plane, especially in laparoscopic context. Greater amount of blood loss in the declamping period ensued in Pringle group because of a longer overall declamping time. Because of the more complex technique and difficult access and deeper regions of the liver, hemostasis at the transection plane is more difficult to be performed in the laparoscopic context than open surgery. More time for performing hemostasis is requested in the laparoscopic context. In particular, when the lesion locates in the right posterior liver, it is a great challenge to surgeons because of difficult access, difficult suturing for hemostasis, a large transection area and its anatomic location, attached to the diaphragm and retroperitoneum and hidden from the surgeon’s view. If bleeding could not be controlled successfully and rapidly before the end of clamping period, hemostasis would be more difficult to be performed during the declamping period. Intermittent vascular occlusion was performed with cycles of 15/5 min of clamp and unclamp times. This time limit might sometimes not be long enough for some complex conditions. Bleeding was often difficult to be controlled before the end of 15-min clamping period. It might cause inadvertent ligation of the major intrahepatic vessels, if hemostasis was performed under a hurried and flustered condition, which was dangerous for cirrhotic patients because ischemic or congestive necrosis would occur in the remnant liver and might cause liver failure. In continuous
Surg Endosc
hemihepatic vascular inflow occlusion, hemostasis could be accurately accomplished without hurry because the clamping period was long enough. The advantages of half-Pringle maneuver are no ischemic reperfusion injury to the remnant liver, avoidance of splanchnic congestion and better hemodynamic tolerability. Bleeding is also one of the important reasons to damage liver function. Less ischemic reperfusion injury and amount of blood loss caused liver function in halfPringle group to have a significant better recovery, which was reflected by the postoperative serum albumin, ALT and AST levels in our study. Surgical trauma caused a dramatic increase in ALT and AST levels in both groups following surgery. The Pringle group was associated with higher ALT and AST levels on PODs 1 and 3, but no significant differences were observed between the two groups, which could be caused by the dramatic variance in ALT and AST levels on PODs 1 and 3 and the statistical variation of small sample size. When the ALT and AST levels in both groups were restored to near normal on POD 7, the Pringle group showed significantly higher ALT and AST levels than the half-Pringle group, which reflected earlier recovery of postoperative liver function in halfPringle group. The Pringle group was also associated with significantly lower albumin levels on PODs 1 and 3, which also demonstrated better recovery in half-Pringle group. CRP is an acute-phase reactant mainly induced by IL-6 during tissue injury [33, 34]. As a key marker, CRP demonstrates a consistent response to surgical stress and provides a reliable measure of the overall acute-phase reaction. Postoperative levels of CRP rise at 4–12 h, peak at 24–72 h and return to baseline at about 2 weeks [33, 34]. In our study, the level of CRP was significantly lower in the half-Pringle group in comparison with the Pringle group, which demonstrated less surgical trauma in the half-Pringle group. Although hemihepatic vascular inflow occlusion using extra-glissonian approach offers the advantages of less blood loss, less injury and better recovery, it is contraindicated for tumors approaching or infiltrating the liver hilum. Moreover, this technique cannot be used in patients with some anatomic variations of the portal vein or hepatic artery. In conclusion, because of the difficulties related to visualization, controlling hemorrhage in the operative field and maintaining hemostasis in the transection plane in laparoscopic liver resections, the ischemic duration should be longer in laparoscopic context than open surgery. Continuous hemihepatic vascular inflow occlusion using extra-glissonian approach would be even more useful and beneficial in the laparoscopic context. On the basis of our findings, we suggest that the maneuver can be recommended for laparoscopic liver resections, especially in some complex conditions.
Acknowledgments This work was supported by Grants from Health Department of Sichuan Province, China, No. 130134, and Doctor Funding of Sichuan Academy of Medical Sciences. Disclosures Drs. Yu Zhang, Hongji Yang, Xiaofan Deng, Yunfei Chen, Shikai Zhu and Chen Kai have no conflict of interest or financial ties to disclose.
References 1. Bai DS, Chen P, Qian JJ, Yao J, Jin SJ, Wang XD, Jiang GQ (2015) Modified laparoscopic hepatectomy for hepatic hemangioma. Surg Endosc. doi:10.1007/s00464-014-4048-y 2. Xiao L, Li JW, Zheng SG (2014) Totally laparoscopic ALPPS in the treatment of cirrhotic hepatocellular carcinoma. Surg Endosc. doi:10.1007/s00464-014-4000-1 3. Shelat VG, Cipriani F, Basseres T, Armstrong TH, Takhar AS, Pearce NW, AbuHilal M (2014) Pure laparoscopic liver resection for large malignant tumors: does size matter? Ann Surg Oncol. doi:10.1245/s10434-014-4107-6 4. Hilal MA, van der Poel MJ, Samim M, Besselink MG, Flowers D, Stedman B, Pearce NW (2015) Laparoscopic liver resection for lesions adjacent to major vasculature: feasibility, safety and oncological efficiency. J Gastrointest Surg. doi:10.1007/s11605014-2739-2 5. Tranchart H, O’Rourke N, Van Dam R, Gaillard M, Lainas P, Sugioka A, Wakabayashi G, Dagher I (2015) Bleeding control during laparoscopic liver resection: a review of literature. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.217 6. Scatton O, Brustia R, Belli G, Pekolj J, Wakabayashi G, Gayet B (2015) What kind of energy devices should be used for laparoscopic liver resection? Recommendations from a systematic review. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.213 7. Otsuka Y, Kaneko H, Cleary SP, Buell JF, Cai X, Wakabayashi G (2015) What is the best technique in parenchymal transection in laparoscopic liver resection? Comprehensive review for the clinical question on the 2nd international consensus conference on laparoscopic liver resection. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.216 8. Mu¨ller MK, Petrowsky H, Clavien PA (2008) Techniques of vascular control and protective strategies for parenchymal transection. In: Lau WY (ed) Hepatocellular carcinoma. World Scientific Publishing, Singapore, pp 507–528 9. Nomi T, Fuks D, Govindasamy M, Mal F, Nakajima Y, Gayet B (2015) Risk factors for complications after laparoscopic major hepatectomy. Br J Surg 102(3):254–260. doi:10.1002/bjs.9726 (Epub 2014 Dec 17) 10. Dua MM, Worhunsky DJ, Hwa K, Poultsides GA, Norton JA, Visser BC (2014) Extracorporeal Pringle for laparoscopic liver resection. Surg Endosc. doi:10.1007/s00464-014-3801-6 11. Nomi T, Fuks D, Agrawal A, Govindasamy M, Araki K, Gayet B (2015) Modified Pringle maneuver for laparoscopic liver resection. Ann Surg Oncol 22(3):852. doi:10.1245/s10434-014-4088-5 12. Jiao H, Tan J, Chu Y, Zhu Z, Dong JH (2014) Modified hepatic vascular occlusion facilitates hepatectomy for malignant hepatic tumor in laparoscopy. Surg Laparosc Endosc Percutan Tech 24(6):506–511. doi:10.1097/SLE.0b013e3182a2b08d 13. Fu SY, Lau WY, Li G-G, Tang QH, Li AJ, Pan ZY, Huang G, Yin L, Wu MC, Lai EC, Zhou WP (2011) A prospective randomized controlled trial to compare Pringle maneuver, hemihepatic vascular inflow occlusion, and main portal vein inflow occlusion in partial hepatectomy. Am J Surg 201:62–69 14. Ni JS, Lau WY, Yang Y, Pan Z-Y, Wang Z-G, Liu H, Wu MC, Zhou WP (2013) A prospective randomized controlled trial to
123
Surg Endosc
15.
16.
17.
18.
19.
20.
21.
22.
23.
compare Pringle maneuver, hemihepatic vascular inflow occlusion, and main portal vein inflow occlusion in partial hepatectomy. J Gastrointest Surg 17:1414–1421 Liang G, Wen T, Yan L, Li BO, Wu G, Yang J, Lu B, Chen Z, Liao Z, Ran S, Yu Z (2009) A prospective randomized comparison of continuous hemihepatic with intermittent total hepatic inflow occlusion in hepatectomy for liver tumors. Hepatogastroenterology 56:745–750 Chen YJ, Zhen ZJ, Chen HW, Lai EC, Deng FW, Li QH, Lau WY (2014) Laparoscopic liver resection under hemihepatic vascular inflow occlusion using the lowering of hilar plate approach. Hepatobiliary Pancreat Dis Int 13:508–512. doi:10. 1016/S1499-3872(14)60293-9 Herman P, Kru¨ger J, Lupinacci R, Coelho F, Perini M (2013) Laparoscopic bisegmentectomy 6 and 7 using a Glissonian approach and a half-Pringle maneuver. Surg Endosc. doi:10.1007/ s00464-012-2681-x Rotellar F, Pardo F, Benito A, Martı´-Cruchaga P, Zozaya G, Pedano N (2012) A novel extra-glissonian approach for totally laparoscopic left hepatectomy. Surg Endosc. doi:10.1007/s00464012-2242-3 Hepp J, Couinaud C (1956) Approach to and use of the left hepatic duct in reparation of the common bile duct. Presse Med 64:947–948 Twaij A, Pucher PH, Sodergren MH, Gall T, Darzi A, Jiao LR (2014) Laparoscopic vs open approach to resection of hepatocellular carcinoma in patients with known cirrhosis: systematic review and meta-analysis. World J Gastroenterol 20:8274–8281. doi:10.3748/wjg.v20.i25.8274 Fuks D, Cauchy F, Fte´riche S, Nomi T, Schwarz L, Dokmak S, Scatton O, Fusco G, Belghiti J, Gayet B, Soubrane O (2015) Laparoscopy decreases pulmonary complications in patients undergoing major liver resection: a propensity score analysis. Ann Surg. doi:10.1097/SLA.0000000000001140 Siniscalchi A, Ercolani G, Tarozzi G, Gamberini L, Cipolat L, Pinna AD, Faenza S (2014) Laparoscopic versus open liver resection: differences in intraoperative and early postoperative outcome among cirrhotic patients with hepatocellular carcinoma—a retrospective observational study. HPB Surg. doi:10. 1155/2014/871251 Yamashita Y, Ikeda T, Kurihara T, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Kawanaka H, Shirabe K, Maehara Y (2014) Long-term favorable surgical results of laparoscopic hepatic resection for hepatocellular carcinoma in patients with cirrhosis: a single-center experience over a 10-year period. J Am Coll Surg 219(6):1117–1123. doi:10.1016/j.jamcollsurg.2014.09.003
123
24. Yoon S, Kim K, Jung D, Yu A, Lee S (2014) Oncological and surgical results of laparoscopic versus open liver resection for HCC less than 5 cm: case-matched analysis. Surg Endosc. doi:10. 1007/s00464-014-3980-1 25. Ahn KS, Kang KJ, Kim YH, Kim TS, Lim TJ (2014) A propensity score-matched case–control comparative study of laparoscopic and open liver resection for hepatocellular carcinoma. J Laparoendosc Adv Surg Tech A 24(12):872–877. doi:10. 1089/lap.2014.0273 26. Coles SR, Besselink MG, Serin KR, Alsaati H, Di Gioia P, Samim M, Pearce NW, Abu Hilal M (2015) Total laparoscopic management of lesions involving liver segment 7. Surg Endosc. doi:10.1007/s00464-014-4052-2 27. Xiang L, Xiao L, Li J, Chen J, Fan Y, Zheng S (2015) Safety and feasibility of laparoscopic hepatectomy for hepatocellular carcinoma in the posterosuperior liver segments. World J Surg. doi:10. 1007/s00268-015-2946-3 28. Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL (2003) Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 138:763–769 29. Figueras J, Lopez-Ben S, Llado L, Rafecas A, Torras J, Ramos E, Fabregat J, Jaurrieta E (2003) Hilar dissection versus the ‘‘glissonean’’ approach and stapling of the pedicle for major hepatectomies: a prospective, randomized trial. Ann Surg 238:111–119 30. Blumgart LH, Hann LE (2000) Surgical and radiologic anatomy of the liver and biliary tract. In: Blumgart LH, Fong Y (eds) Surgery of the liver and biliary tract, chap 1, 3rd edn. WB Saunders Co. Ltd., London, pp 21–22 31. Giordano M, Lopez-Ben S, Codina-Barreras A, Pardina B, Falgueras L, Torres-Bahi S, Albiol M, Castro E, Figueras J (2010) Extra-glissonian approach in liver resection. HPB (Oxford) 12:94–100 32. Tranchart H, Gaillard M, Chirica M, Ferretti S, Perlemuter G, Naveau S, Dagher I (2014) Multivariate analysis of risk factors for postoperative complications after laparoscopic liver resection. Surg Endosc. doi:10.1007/s00464-014-3965-0 33. Jiang G-Q, Chen P, Qian J-J, Yao J, Wang X-D, Jin S-J, Bai D-S (2014) Perioperative advantages of modified laparoscopic vs open splenectomy and azygoportal disconnection. World J Gastroenterol 20(27):9146–9153. doi:10.3748/wjg.v20.i27.9146 34. Muscari A, Collini A, Fabbri E, Giovagnoli M, Napoli C, Rossi V, Vizioli L, Bonfiglioli A, Magalotti D, Puddu GM, Zoli M (2014) Changes of liver enzymes and bilirubin during ischemic stroke: mechanisms and possible significance. BMC Neurol 14:122. doi:10.1186/1471-2377-14-122
and Other Interventional Techniques
Intermittent Pringle maneuver versus continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection Yu Zhang1 • Hongji Yang1 • Xiaofan Deng1 • Yunfei Chen1 • Shikai Zhu1 Chen Kai1
•
Received: 12 February 2015 / Accepted: 8 May 2015 Ó Springer Science+Business Media New York 2015
Abstract Background Despite accumulated experience and advancing techniques for laparoscopic hepatectomy, bleeding remains the major concern during parenchymal transection. The vascular inflow control technique is still important to decrease intraoperative blood loss. The objective of this study was to compare intermittent Pringle with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection. Methods Between January 2011 and January 2015, a total of 79 consecutive patients with tumors locating either in the right or in the left hemiliver were included into this retrospective study (45 in the Pringle group vs. 34 in the half-Pringle group). Preoperative clinical characteristics, intraoperative details, postoperative complications and outcomes of patients were compared. Results The two groups were well matched according to clinical characteristics, tumor features, types of liver resection and histopathology (P [ 0.05). The mean operative time (247.5 ± 61.3 vs. 221.4 ± 48.7 min, P = 0.0446), ischemic duration (62.8 ± 28.3 vs. 44.1 ± 20.5 min, P = 0.0017) and overall declamping time (21.2 ± 8.2 vs. 0.9 ± 1.9 min, P \ 0.05) were significantly longer in the Pringle group
Yu Zhang and Hongji Yang have contributed equally to this work. & Yu Zhang [email protected] & Hongji Yang [email protected] 1
The Third Department of Hepatobiliary Surgery, Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), Chinese Academy of Sciences, No. 32 West Second Section, First Ring Road, Chengdu 610072, Sichuan, People’s Republic of China
than in the half-Pringle group. The mean amount of intraoperative blood loss (568.2 ± 325.1 vs. 420.7 ± 307.2 mL, P = 0.0444) and transfusion (266.1 ± 123.4 vs. 203.2 ± 144.6 mL, P = 0.0406) were significantly greater in the Pringle group. The overall operative morbidity rate was significantly higher in the Pringle group (40 vs. 17.6 %, P = 0.0324). The Pringle group was associated with significantly higher alanine aminotransferase and aspartate transaminase levels on postoperative day (POD) 7 and lower albumin levels on PODs 1 and 3 (P \ 0.05). The C-reactive protein levels were significantly higher in the Pringle group than in the half-Pringle group on POD 1 (37.5 ± 21.4 vs. 28.2 ± 19.0 mg/L, P = 0.0484), POD 3 (114.0 ± 53.4 vs. 90.6 ± 47.9 mg/L, P = 0.0474) and POD 7 (54.9 ± 29.8 vs. 40.1 ± 26.4 mg/L, P = 0.0245). Conclusion Continuous hemihepatic vascular inflow occlusion using extra-glissonian approach offers the advantages of less operative time and blood loss, less injury and better recovery in laparoscopic liver resection. Keywords Extra-glissonian approach Laparoscopic liver resection Liver neoplasm Pringle maneuver Hemihepatic vascular inflow occlusion Despite accumulated experience and advancing techniques for laparoscopic hepatectomy [1–4], bleeding remains the major concern during parenchymal transection [5–7]. Excessive blood loss and the need for blood transfusions are predictors of poor outcome for both noncirrhotic and cirrhotic liver resections [8, 9]. The vascular inflow control technique is still important to decrease intraoperative blood loss [10–12]. Some randomized controlled trials have been carried out to evaluate the impact of Pringle maneuver (total vascular inflow occlusion) and intermittent [13, 14] or continuous [15] hemihepatic
123
Surg Endosc
vascular inflow occlusion in open liver resection. These trials showed that total vascular inflow occlusion could be performed, but ischemic reperfusion injuries could lead to higher postoperative morbidity. However, hemihepatic inflow occlusion could decrease the amount of liver parenchyma submitted to reperfusion damage and offer the advantage of reduced blood loss [13, 14]. Some studies have demonstrated that laparoscopic liver resection with the intermittent half-Pringle maneuver is feasible and safe [16] and that laparoscopic glissonian approach is gaining popularity because it may reduce the time of operation and avoids dangerous and tedious laparoscopic dissection of liver hilum [17, 18]. However, continuous half-Pringle maneuver in laparoscopic liver resection has been reported limitedly. Because of the more technical difficulty associated with bleeding control, hemostasis at the transection plane, hilar dissection, the risk of gas embolism and deeper regions of the liver, we feel that continuous hemihepatic inflow occlusion could be even more useful in the laparoscopic context, especially using extra-glissonian approach. To our knowledge, there has been almost no study to compare intermittent Pringle maneuver with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach (half-Pringle maneuver) in laparoscopic liver resection. The objective of this study was to compare intermittent Pringle with continuous hemihepatic vascular inflow occlusion using extra-glissonian approach in laparoscopic liver resection.
Materials and methods Patients Between January 2011 and January 2015, a total of consecutive 79 patients with tumors locating either in the right or in the left hemiliver were considered to be included into this study, who underwent laparoscopic hepatotomy at the Third Department of Hepatobiliary Surgery, Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), Chinese Academy of Sciences. Data on these patients were analyzed retrospectively from a prospective database. Of the total 79 laparoscopic liver resections, 45 cases were performed by intermittent Pringle maneuver (the Pringle group), and the other 34 cases were performed by continuous hemihepatic vascular inflow occlusion using extra-glissonian approach (the half-Pringle group). The indications for the two groups were determined based on the same criteria: (1) elective liver resection; (2) tumors that were located either in the right or in the left hemiliver; (3) no major vascular involvement, and no tumor close to or even infiltrating the liver hilum; (4) tumor
123
size B8 cm, and extent of partial hepatectomy was a hemihepatectomy or less; (5) no concomitant surgical procedures except cholecystectomy; and (6) well-compensated chronic liver disease (Child-Pugh class A or B) without signs of severe portal hypertension (esophageal varices B F2). The preoperative workup consisted of a specified protocol including blood examinations, chest X-ray, abdominal ultrasound and contrast computed tomography scan. In selected cases, we performed spirometry, esophagogastroduodenoscopy and angiomagnetic resonance imaging. Liver function was assessed by the Child-Pugh grading. Laboratory blood tests included hemoglobin (HGB), white blood cell (WBC), platelet (PLT), albumin (Alb), alanine aminotransferase (ALT), aspartate transaminase (AST), serum total bilirubin (TBIL), prothrombin time (PT), international normalized ration (INR), HBsAg, antibodies to hepatitis C, serum alpha-fetoprotein (AFP), carcinoembryonic antigen (CEA), carbohydrate antigen 19-9 (CA199) and C-reactive protein (CRP). All procedures were performed after informed consents were obtained. All operations were performed by the same surgical team. This study was approved by the ethical committee of the Sichuan Academy of Medical Sciences (Sichuan Provincial People’s Hospital), and it followed the ethical guidelines of the 1975 Declaration of Helsinki. Surgical procedure After appropriate preoperative preparation, the patient was taken to the operating room for laparoscopic hepatotomy. The patients received general anesthesia. When tumors located in the right hemiliver, the patients were placed in the left semidecubitus position with the right side elevated approximately 30°. Generally, five ports were used. The first trocar (12 mm) was inserted at the right-upper umbilicus for placement of a 10-mm 30° laparoscope. Four other trocars were inserted at the subxiphoid position (5 mm), at 5 cm superior to the umbilicus on the midline (12 mm), at 5 cm below the costal margin on the right midclavicular line (12 mm) and 2 cm below the costal margin on the right axillary line (5 mm) (Fig. 1). When tumors located in the left hemiliver, the patients were placed in the right semidecubitus position with the left side elevated approximately 15°. Five ports were used. The first trocar (12 mm) was inserted at the left of umbilicus for placement of a 10-mm 30° laparoscope. Four other trocars were inserted at 5 cm right superior to the umbilicus, at 2 cm below the costal margin on either the right or the left midclavicular line (5 and 12 mm) and 2 cm below the costal margin on the right axillary line (5 mm) (Fig. 2). After placing all trocars successfully, the operating table was tilted slightly to the reverse Trendelenburg position.
Surg Endosc
Fig. 2 Port placement When tumors located in the left hemiliver
together with the sling could be clamped with a Pean clamp to prevent gas leakage and sling slipping and the internal rubber catheter could protect hepatoduodenal ligament from injury by the hard catheter. Tightening of the sling and clamping of rubber catheter on the external end would result in vascular inflow occlusion. Tightening or loosening of the sling would result in clamping or unclamping of the entire liver. Intermittent vascular occlusion was performed with cycles of 15/5 min of clamp and unclamp times. For hemihepatic vascular inflow occlusion, the hilar plate was lowered, similar to the open technique as described by Hepp and Couinaud [19], to expose the confluence of the right and left portal pedicles by lifting the segment 4b of the liver (quadrant lobe) upward and incising the Glisson’s capsule at its base. Without entering the liver substance, a space could be developed by bluntly dissecting between the liver substance and the hilar plate. Either the right or the left portal pedicle was isolated en bloc and was encircled with a tourniquet to enable performance of a half-Pringle maneuver (Figs. 4, 5). Similar to the Pringle maneuver, tightening or loosening of the tourniquet would result in clamping or unclamping of the corresponding hemiliver. Separate clamping of the accessory left hepatic artery was necessary when it was present for control of the vascular inflow to the left hemiliver. The hemihepatic vascular occlusion was continuous if the parenchymal transection time was not more than 60 min, or else 5 min of reperfusion was required, despite which occurred seldom. The half-Pringle maneuver resulted in a visible line of ischemic demarcation along the main liver fissure (Cantlie line) (Fig. 6). The parenchymal transection was performed using the ultrasonic dissector (Harmonic Scalpel; Ethicon EndoSurgery). Bipolar electrocoagulation was used for minor bleeding. Intraparenchymal control of the major vessels was obtained with titanium clips, vascular locks or suturing
Exploration of the abdominal cavity was performed routinely. Intraoperative ultrasound was performed to confirm the extension of the tumor, the number of lesions and their position in relation to the main hepatic structures. The area to be resected was marked by electrocautery. If necessary, cholecystectomy was carried out. For Pringle maneuver, the avascular lesser omentum was divided, and a sling was placed around the entire hepatoduodenal ligament and passed through a 16-Fr hard catheter for use as a tourniquet to enable performance of a Pringle maneuver. Both ends of the hard catheter were connected by a 2-cm soft rubber catheter. The internal end of the catheter was close to the pedicle and the external end was extracorporeal, allowing for easy external occlusion (Fig. 3). When clamping, the external rubber catheter
Fig. 3 Pringle maneuver
Fig. 1 Port placement When tumors located in the right hemiliver
123
Surg Endosc
using prolene sutures. Linear laparoscopic staplers (Echelon 60 ENDOPATH Stapler, Ethicon Endo-Surgery, LLC, Cincinnati, OH, USA) were used to transect the major vascular structures, including the left/right hepatic pedicle, left/right hepatic vein and inferior right hepatic vein. The central venous pressure was kept below 5 mmHg during liver parenchymal transection [5], and continuous carbon dioxide pneumoperitoneum pressure was induced at a pressure lower than 12 mmHg to reduce the risk of gas embolism. Postoperative management
Fig. 4 Right portal pedicle was isolated en bloc and encircled with a sling
All patients received the same postoperative care by the same team of surgeons. Postoperative parameters of hepatic damage and recovery, including serum TBIL, ALT, AST, Alb, creatinine, PT, INR and CRP, were measured on postoperative days (PODs) 1, 3 and 7. The abdominal ultrasound examination was repeated on POD 7. Statistical methods Results were expressed as mean ± standard deviation and were analyzed by paired-sample t (t0 ) test. And the v2 test (with continuity corrected v2 if the expected count was \5) or the Fisher exact test was appropriate for categorical data. All calculations were performed using the SPSS 17.0 statistical software. Results with P value \0.05 (paired-tailed test) were considered statistically significant.
Results Fig. 5 Left portal pedicle was isolated en bloc and encircled with a sling
Baseline characteristics and surgical feasibility The two groups were well matched according to clinical characteristics, tumor features, types of liver resection and histopathology (P [ 0.05). The preoperative clinical and laboratory parameters were comparable in both groups of patients (Table 1). The mean size of the tumors was 4.4 ± 2.3 cm in the Pringle group, which was comparable to that in the half-Pringle group (4.6 ± 2.5 cm) (P = 0.7134). There were no significant differences between the two groups in terms of types of liver resection performed, percentage of main tumor with satellite nodules and patients with portal hypertension (Table 1). The histopathology of tumor or nontumorous liver was comparable between the two groups of patients (Table 2). Intraoperative results
Fig. 6 Visible line of ischemic demarcation along the main liver fissure (Cantlie line)
123
All of the patients underwent R0 resection. There was no margin invasion in the both groups. The tumor-free resection margin was comparable between the two groups of patients. Of
Surg Endosc Table 1 Clinical characteristics of patients
Pringle (n = 45)
Half-Pringle (n = 34)
t (v2)
P value
0.0599
0.8067
Sex M
29
21
F
16
13
Age (years)
47.3 ± 11.4
49.8 ± 13.6
0.8879
0.3773
BMI
22.4 ± 4.2
23.2 ± 3.8
0.8729
0.3855
WBC count (109/L)
5.2 ± 2.5
4.8 ± 2.8
0.6686
0.5057
PLT count (109/L)
168.4 ± 66.4
186.9 ± 73.5
1.1709
0.2452
HGB (g/L)
112.3 ± 28.5
123.8 ± 31.4
1.6996
0.0932
Grade A, n
38
30
0.0236
0.8778
Grade B, n
Child-Pugh classification 7
4
ALT (U/L)
41.3 ± 27.8
46.0 ± 25.3
0.773
0.4419
AST (U/L)
34.9 ± 18.5
36.7 ± 19.3
0.4203
0.6754
TBIL (lmol/L)
15.4 ± 5.1
16.6 ± 4.3
1.1063
0.2720
Alb (g/L) INR
39.7 ± 4.4 1.06 ± 0.18
41.3 ± 5.1 1.08 ± 0.21
1.4941 0.455
0.1392 0.6504
Creatinine (lmol/L)
65.3 ± 17.6
67.5 ± 16.8
0.5609
0.5765
CRP (mg/L)
7.9 ± 6.7
7.4 ± 7.1
0.3201
0.7498
Tumor size (cm)
4.4 ± 2.3
4.6 ± 2.5
0.3686
0.7134
Main tumor with satellite nodules, n
3
2
0.1055
0.7453
Patients with portal hypertension, n
7
5
0.0109
0.9170
AST aspartate transaminase, ALT alanine aminotransferase, Alb albumin, TBIL serum total bilirubin, INR international normalized ration, HGB hemoglobin, WBC white blood cell, CRP C-reactive protein
the total 79 cases, three cases were converted from a laparoscopic to an open procedure due to uncontrollable bleeding. The percentage of conversions was comparable between the two groups of patients (P [ 0.05). The mean operative time (247.5 ± 61.3 vs. 221.4 ± 48.7 min, P = 0.0446), ischemic duration (62.8 ± 28.3 vs. 44.1 ± 20.5 min, P = 0.0017) and overall declamping time (21.2 ± 8.2 vs. 0.9 ± 1.9 min, P \ 0.05) in the Pringle group were significantly longer than those in the half-Pringle group. The mean amount of intraoperative blood loss in the Pringle group was significantly greater than that in the half-Pringle group (568.2 ± 325.1 vs. 420.7 ± 307.2 mL, P = 0.0444). As a result, there was a significantly greater volume of intraoperative blood transfusion in the Pringle group (266.1 ± 123.4 vs. 203.2 ± 144.6 mL, P = 0.0406). No differences were observed in the percentage of patients transfused and the volume of crystalloid administered (P [ 0.05). In the halfPringle group, the mean time taken to prepare the hemihepatic vascular inflow occlusion was 19.3 min (range 8–27 min), which decreased to \15 min (range 8–15 min) in the last 15 cases of half-Pringle procedures. Postoperative complications and outcomes In this study, both groups had no perioperative mortality, which was defined as death within 90 days of surgery or death during the same hospital admission of surgery. There
was no evidence of intraoperative or postoperative gas embolism in any of the patients. No bile duct injury occurred in either group. Postoperative hospital stay was similar in the two groups (P [ 0.05). Postoperative ascites was defined by an abdominal drainage output more than 500 mL/day, or required treatment to be controlled. Hepatic insufficiency was defined as a PT of more than 50 % of normal and/or by serum bilirubin of more than 50 lmol/L on POD 7 or thereafter and/or encephalopathy. There was no significant difference in any type of complications (P [ 0.05); however, the overall operative morbidity rate in the Pringle group was significantly higher than that in the half-Pringle group (40 vs. 17.6 %, P = 0.0324). More details are reported in Table 3. The liver functional status on PODs 1, 3 and 7 as reflected by the postoperative changes of albumin, serum bilirubin, transaminase levels and INR is shown in Table 3. ALT and AST levels in both groups increased dramatically following surgery. The mean ALT level on POD 1 was about 16 times and the mean AST level on POD 1 was about 17 times comparing to preoperative levels in the Pringle group. The mean ALT level on POD 1 was 12 times and the mean AST level on POD 1 was about 13 times comparing to preoperative levels in the half-Pringle group. No significant differences were observed in ALT and AST levels on PODs 1 and 3 between the two groups (P [ 0.05). On POD 7, the ALT and AST levels in
123
Surg Endosc Table 2 Intraoperative detail of patients t/t0 (v2)
P Value
1
0.0527
0.8184
5
0.0034
0.9536
Pringle (n = 45)
Half-Pringle (n = 34)
Segment III
3
Segment II ? III
8
Type of liver resection, n
Segment II ? III ? IV
4
4
0.0018
0.9658
Segment V
5
4
0.0713
0.7894
Segment VI
5
3
0.0018
0.9658
Segment VII
3
4
0.1519
0.6968
Segment V ? VI
6
4
0.0180
0.8933
Segment VI ? VII
2
2
0.0527
0.8184
Segment V ? VI ? VII
4
3
0.1519
0.6968
5
4
0.0713
0.7894
Hepatocellular carcinoma
22
19
0.3794
0.5379
Cholangiocarcinoma
4
2
0.0050
0.9437
Segment V ? VI ? VII ? VIII Pathologic diagnosis, n
Mixed hepatocholangiocarcinoma
2
1
0.0617
0.8039
Metastases of colorectal carcinoma
3
3
0.0050
0.9437
Hemangioma
10
8
0.0188
0.8909
Focal nodular hyperplasia
2
0
Stromal tumor
2
1
0.5034 0.0617
0.8039
Nontumorous liver, n Normal
20
13
0.3070
0.5795
Chronic hepatitis
6
5
0.0236
0.8778
Cirrhosis
19
16
0.1836
0.6683
38
29
0.0109
0.9170
0.0617 2.0421
0.8039 0.0446
Tumor-free resection margin [1 cm 0–1 cm Conversion to open liver resection, n Operation time(range) (min)
7
5
2 247.5 ± 61.3 (90–380)
1 221.4 ± 48.7 (80–335)
Ischemic duration (range) (min)
62.8 ± 28.3 (30–120)
44.1 ± 20.5 (26–80)
Overall declamping time(range) (min)
21.2 ± 8.2 (5–35)
0.9 ± 1.9 (0–5)
3.2587 16.0466
0.0017 \0.05
Intraoperative blood loss (mL)
568.2 ± 325.1
420.7 ± 307.2
2.0441
0.0444
Intraoperative blood transfusion (mL)
266.1 ± 123.4
203.2 ± 144.6
2.0828
0.0406
Patients transfused, n
11
7
0.1637
0.6858
2737 ± 1113
2556 ± 1035
0.7374
0.4631
Crystalloid perfused (mL)
both groups were restored to near normal; however, the Pringle group was associated with significantly higher ALT and AST levels than the half-Pringle group (P \ 0.05). The indication to use intravenous albumin was albumin level \25 g/L together with ascites or hepatic insufficiency after operation in this study. The percentage of patients supplemented with intravenous albumin was similar in the two groups (P [ 0.05). The Pringle group was also associated with significantly lower albumin levels on PODs 1 and 3 (P \ 0.05). There were no significant differences in the bilirubin and the creatinine levels between the two groups (P [ 0.05). Mean CRP concentrations were similar preoperatively (P [ 0.05), and there was an increase in the plasma concentration of CRP in both groups following surgery. The
123
mean CRP levels were significantly higher in the Pringle group than in the half-Pringle group on POD 1 (37.5 ± 21.4 vs. 28.2 ± 19.0 mg/L, P = 0.0484), POD 3 (114.0 ± 53.4 vs. 90.6 ± 47.9 mg/L, P = 0.0474) and POD 7 (54.9 ± 29.8 vs. 40.1 ± 26.4 mg/L, P = 0.0245).
Discussion Laparoscopic liver resection is safe and may provide improved patient outcomes when compared to the open technique [20–23]. Long-term results show that oncological benefits of a laparoscopic approach are similar to open surgery [23–25]. With the improvement in laparoscopic
Surg Endosc Table 3 Postoperative complications and outcomes
Pringle (n = 45)
Half-Pringle (n = 34)
t (v2)
P value
Postoperative complications Postoperative bleeding, n
1
0
1.0000
Hepatic insufficiency, n
2
0
0.5034
Surgical site infections, n
1
1
1.0000
Cardiac insufficiency, n
1
0
1.0000
Creatinine transient elevation
1
0
Bile leakage, n
2
1
0.0617
Pulmonary infection, n
2
1
0.0617
0.8039
Ascites, n
5
2
0.1680
0.6819
Pulmonary effusion, n
6
0.0713
0.7894
1.0000
3 a
b
0.8039
Operative morbidity, n (%)
18 (40.0 %)
6 (17.6 %)
4.5752
0.0324
Patients using intravenous albumin, n (%)
4
1
0.3701
0.5429
656.5 ± 487.3 601.3 ± 402.8
563.8 ± 378.5 490.3 ± 312.2
0.9189 1.332
0.3610 0.1868
Postoperative outcome POD 1 ALT (U/L) AST (U/L) TBIL (lmol/L)
15.3 ± 7.8
13.3 ± 8.3
1.0977
0.2757
Alb (g/L)
27.5 ± 3.8
29.3 ± 3.3
2.2039
0.0305
INR
1.10 ± 0.54
1.08 ± 0.61
0.1541
0.8779
Creatinine (lmol/L)
65.3 ± 17.6
67.5 ± 16.8
0.5609
0.5765
CRP(mg/L)
37.5 ± 21.4
28.2 ± 19.0
2.0057
0.0484
POD 3 ALT (U/L)
237.4 ± 156.7
218.9 ± 143.5
0.5385
0.5918
AST (U/L)
284.3 ± 177.8
265.1 ± 183.7
0.4685
0.6407
TBIL (lmol/L)
35.3 ± 9.8
33.6 ± 7.4
0.8452
0.4006
Alb(g/L)
31.4 ± 4.7
33.8 ± 5.2
2.1465
0.0350
INR
1.22 ± 0.62
1.20 ± 0.58
0.1459
0.8844
Creatinine (lmol/L)
55.4 ± 13.7
51.2 ± 15.6
1.2708
0.2076
CRP (mg/L)
114.0 ± 53.4
90.6 ± 47.9
2.0146
0.0474
ALT (U/L) AST (U/L)
67.7 ± 28.4 74.4 ± 34.6
54.3 ± 21.5 58.9 ± 26.7
2.2972 2.1684
0.0243 0.0332
TBIL (lmol/L)
18.4 ± 7.7
16.5 ± 8.2
1.056
0.2943
Alb (g/L)
31.8 ± 5.1
32.7 ± 4.6
0.8096
0.4206 0.7365
POD 7
INR
1.13 ± 0.55
1.0 9 ± 0.48
0.3378
Creatinine (lmol/L)
47.9 ± 17.8
45.5 ± 20.1
0.5612
0.5763
CRP(mg/L)
54.9 ± 29.8
40.1 ± 26.4
2.294
0.0245
8.8 ± 2.7
8.4 ± 2.3
0.694
0.4897
Postoperative hospital stay(days) a
Twenty-one complications occurred in 18 patients
b
Eight complications occurred in six patients
equipments [6, 7] and the accumulation of clinical experience in laparoscopic and hepatic surgery, the indications for laparoscopic liver resection are expanding, including the type of resection and the size or location of the tumor [26, 27]. Although many limitations have been overcome, bleeding is still the most important problem that hinders the development of laparoscopic liver resection. Surgeons still
face challenging resections that require specific and innovative maneuvers to decrease intraoperative blood loss, as bleeding together with subsequent blood transfusion increases postoperative morbidity and mortality and enhances tumor recurrence in patients undergoing hepatectomy for liver malignancy [8, 9]. Pringle maneuver is the traditional and the most commonly used method to decrease blood loss during hepatic
123
Surg Endosc
parenchymal transection because of its effectiveness and simplicity, but can be associated with prolonged ischemic time. Laurent et al. [28] reported that laparoscopic liver resections are associated with higher ischemic times. Fu et al. [13] reported that both Pringle and half-Pringle maneuvers were safe and efficacious in reducing blood loss. Patients subjected to intermittent hemihepatic vascular inflow occlusion responded better than those with Pringle maneuver in terms of earlier recovery of postoperative liver function. And Ni et al.’s study [14] confirmed that in patients with HCC with cirrhosis, intermittent hemihepatic vascular inflow occlusion was still a better inflow occlusion method than Pringle maneuver. Liang et al. [15] reported a prospective randomized trial to compare continuous hemihepatic with intermittent total hepatic inflow occlusion in open hepatectomy. Liang et al. [15] suggest that continuous hemihepatic inflow occlusion is safe and effective, similar to intermittent total hepatic inflow occlusion, and it is recommended for complex liver resection. The above-mentioned studies were all carried out to compare the impact of Pringle maneuver with hemihepatic vascular inflow occlusion in open liver resections. [13–15]. Chen et al. [16] have reported half-Pringle maneuver using extra-glissonian approach in laparoscopic liver resections. However, intermittent half-Pringle maneuver was performed in his study (15/5 min), instead of continuous half-Pringle maneuver. To the best of our knowledge, our study is the first specific series to compare intermittent Pringle with continuous hemihepatic inflow occlusion using extra-glissonian approach in laparoscopic liver resections. Previous experience in more simple laparoscopic hepatic resections is necessary to any laparoscopic complex liver resection. Similarly, we consider indispensable previous experience with the extra-glissonian approach in open surgery. It is evident that no attempt should be made without experience performing open extra-glissonian approach. But if meeting these two requirements, the technique is surprisingly simple and effective. The procedure of hemihepatic inflow occlusion using extra-glissonian approach in laparoscopic liver resections required experience of the surgeon. Once the surgeon had acquired the technique, the preparation of the hemihepatic vascular inflow occlusion could be accomplished in about 15 min. It took\15 min (range 8–15 min) in the last 15 cases of halfPringle procedures in our study. Once the portal pedicles were exposed, either the left or the right portal pedicle could be encircled with a sling. Tightening or loosening of the sling would result in clamping or unclamping of the corresponding hemiliver. The procedure using extra-glissonian approach without entering the liver substance can be performed easily and rapidly, with minimal bleeding by blunt maneuvers without hilar dissection, and is better than
123
separate isolation of the hepatic artery, duct and portal vein [29]. The extra-glissonian approach allows safe en masse control of the portal structures without prolonged dissection, since it is exceptional (in 1 % of case) to have any vascular interposition between the inferior surface of the liver and the hilar plate [30]. We did not encounter any difficulties or excessive bleeding during preparation of the hemihepatic vascular inflow occlusion in this study. The extra-glissonian approach has been proven useful in open hepatectomies [31], which has also been used in different laparoscopic surgical procedures [16–18]. The advantages of this approach may be enhanced in the laparoscopic context. Tranchart [32] reported that in the patients that underwent laparoscopic liver resection for malignancy, operative time was the sole independent predictor of postoperative morbidity. Postoperative complication rate increases by 60 % with each additional operative hour during laparoscopic liver resection [32]. The mean operative time was significantly longer in the Pringle group than in the halfPringle group, which could be caused by the longer ischemic duration and overall time in declamping periods in the Pringle group. Another important reason was that surgeons had to spend more time controlling bleeding in the Pringle group. The amount of blood loss in the declamping periods was great, because it is very difficult to perform total compression of a wide transection plane, especially in laparoscopic context. Greater amount of blood loss in the declamping period ensued in Pringle group because of a longer overall declamping time. Because of the more complex technique and difficult access and deeper regions of the liver, hemostasis at the transection plane is more difficult to be performed in the laparoscopic context than open surgery. More time for performing hemostasis is requested in the laparoscopic context. In particular, when the lesion locates in the right posterior liver, it is a great challenge to surgeons because of difficult access, difficult suturing for hemostasis, a large transection area and its anatomic location, attached to the diaphragm and retroperitoneum and hidden from the surgeon’s view. If bleeding could not be controlled successfully and rapidly before the end of clamping period, hemostasis would be more difficult to be performed during the declamping period. Intermittent vascular occlusion was performed with cycles of 15/5 min of clamp and unclamp times. This time limit might sometimes not be long enough for some complex conditions. Bleeding was often difficult to be controlled before the end of 15-min clamping period. It might cause inadvertent ligation of the major intrahepatic vessels, if hemostasis was performed under a hurried and flustered condition, which was dangerous for cirrhotic patients because ischemic or congestive necrosis would occur in the remnant liver and might cause liver failure. In continuous
Surg Endosc
hemihepatic vascular inflow occlusion, hemostasis could be accurately accomplished without hurry because the clamping period was long enough. The advantages of half-Pringle maneuver are no ischemic reperfusion injury to the remnant liver, avoidance of splanchnic congestion and better hemodynamic tolerability. Bleeding is also one of the important reasons to damage liver function. Less ischemic reperfusion injury and amount of blood loss caused liver function in halfPringle group to have a significant better recovery, which was reflected by the postoperative serum albumin, ALT and AST levels in our study. Surgical trauma caused a dramatic increase in ALT and AST levels in both groups following surgery. The Pringle group was associated with higher ALT and AST levels on PODs 1 and 3, but no significant differences were observed between the two groups, which could be caused by the dramatic variance in ALT and AST levels on PODs 1 and 3 and the statistical variation of small sample size. When the ALT and AST levels in both groups were restored to near normal on POD 7, the Pringle group showed significantly higher ALT and AST levels than the half-Pringle group, which reflected earlier recovery of postoperative liver function in halfPringle group. The Pringle group was also associated with significantly lower albumin levels on PODs 1 and 3, which also demonstrated better recovery in half-Pringle group. CRP is an acute-phase reactant mainly induced by IL-6 during tissue injury [33, 34]. As a key marker, CRP demonstrates a consistent response to surgical stress and provides a reliable measure of the overall acute-phase reaction. Postoperative levels of CRP rise at 4–12 h, peak at 24–72 h and return to baseline at about 2 weeks [33, 34]. In our study, the level of CRP was significantly lower in the half-Pringle group in comparison with the Pringle group, which demonstrated less surgical trauma in the half-Pringle group. Although hemihepatic vascular inflow occlusion using extra-glissonian approach offers the advantages of less blood loss, less injury and better recovery, it is contraindicated for tumors approaching or infiltrating the liver hilum. Moreover, this technique cannot be used in patients with some anatomic variations of the portal vein or hepatic artery. In conclusion, because of the difficulties related to visualization, controlling hemorrhage in the operative field and maintaining hemostasis in the transection plane in laparoscopic liver resections, the ischemic duration should be longer in laparoscopic context than open surgery. Continuous hemihepatic vascular inflow occlusion using extra-glissonian approach would be even more useful and beneficial in the laparoscopic context. On the basis of our findings, we suggest that the maneuver can be recommended for laparoscopic liver resections, especially in some complex conditions.
Acknowledgments This work was supported by Grants from Health Department of Sichuan Province, China, No. 130134, and Doctor Funding of Sichuan Academy of Medical Sciences. Disclosures Drs. Yu Zhang, Hongji Yang, Xiaofan Deng, Yunfei Chen, Shikai Zhu and Chen Kai have no conflict of interest or financial ties to disclose.
References 1. Bai DS, Chen P, Qian JJ, Yao J, Jin SJ, Wang XD, Jiang GQ (2015) Modified laparoscopic hepatectomy for hepatic hemangioma. Surg Endosc. doi:10.1007/s00464-014-4048-y 2. Xiao L, Li JW, Zheng SG (2014) Totally laparoscopic ALPPS in the treatment of cirrhotic hepatocellular carcinoma. Surg Endosc. doi:10.1007/s00464-014-4000-1 3. Shelat VG, Cipriani F, Basseres T, Armstrong TH, Takhar AS, Pearce NW, AbuHilal M (2014) Pure laparoscopic liver resection for large malignant tumors: does size matter? Ann Surg Oncol. doi:10.1245/s10434-014-4107-6 4. Hilal MA, van der Poel MJ, Samim M, Besselink MG, Flowers D, Stedman B, Pearce NW (2015) Laparoscopic liver resection for lesions adjacent to major vasculature: feasibility, safety and oncological efficiency. J Gastrointest Surg. doi:10.1007/s11605014-2739-2 5. Tranchart H, O’Rourke N, Van Dam R, Gaillard M, Lainas P, Sugioka A, Wakabayashi G, Dagher I (2015) Bleeding control during laparoscopic liver resection: a review of literature. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.217 6. Scatton O, Brustia R, Belli G, Pekolj J, Wakabayashi G, Gayet B (2015) What kind of energy devices should be used for laparoscopic liver resection? Recommendations from a systematic review. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.213 7. Otsuka Y, Kaneko H, Cleary SP, Buell JF, Cai X, Wakabayashi G (2015) What is the best technique in parenchymal transection in laparoscopic liver resection? Comprehensive review for the clinical question on the 2nd international consensus conference on laparoscopic liver resection. J Hepatobiliary Pancreat Sci. doi:10.1002/jhbp.216 8. Mu¨ller MK, Petrowsky H, Clavien PA (2008) Techniques of vascular control and protective strategies for parenchymal transection. In: Lau WY (ed) Hepatocellular carcinoma. World Scientific Publishing, Singapore, pp 507–528 9. Nomi T, Fuks D, Govindasamy M, Mal F, Nakajima Y, Gayet B (2015) Risk factors for complications after laparoscopic major hepatectomy. Br J Surg 102(3):254–260. doi:10.1002/bjs.9726 (Epub 2014 Dec 17) 10. Dua MM, Worhunsky DJ, Hwa K, Poultsides GA, Norton JA, Visser BC (2014) Extracorporeal Pringle for laparoscopic liver resection. Surg Endosc. doi:10.1007/s00464-014-3801-6 11. Nomi T, Fuks D, Agrawal A, Govindasamy M, Araki K, Gayet B (2015) Modified Pringle maneuver for laparoscopic liver resection. Ann Surg Oncol 22(3):852. doi:10.1245/s10434-014-4088-5 12. Jiao H, Tan J, Chu Y, Zhu Z, Dong JH (2014) Modified hepatic vascular occlusion facilitates hepatectomy for malignant hepatic tumor in laparoscopy. Surg Laparosc Endosc Percutan Tech 24(6):506–511. doi:10.1097/SLE.0b013e3182a2b08d 13. Fu SY, Lau WY, Li G-G, Tang QH, Li AJ, Pan ZY, Huang G, Yin L, Wu MC, Lai EC, Zhou WP (2011) A prospective randomized controlled trial to compare Pringle maneuver, hemihepatic vascular inflow occlusion, and main portal vein inflow occlusion in partial hepatectomy. Am J Surg 201:62–69 14. Ni JS, Lau WY, Yang Y, Pan Z-Y, Wang Z-G, Liu H, Wu MC, Zhou WP (2013) A prospective randomized controlled trial to
123
Surg Endosc
15.
16.
17.
18.
19.
20.
21.
22.
23.
compare Pringle maneuver, hemihepatic vascular inflow occlusion, and main portal vein inflow occlusion in partial hepatectomy. J Gastrointest Surg 17:1414–1421 Liang G, Wen T, Yan L, Li BO, Wu G, Yang J, Lu B, Chen Z, Liao Z, Ran S, Yu Z (2009) A prospective randomized comparison of continuous hemihepatic with intermittent total hepatic inflow occlusion in hepatectomy for liver tumors. Hepatogastroenterology 56:745–750 Chen YJ, Zhen ZJ, Chen HW, Lai EC, Deng FW, Li QH, Lau WY (2014) Laparoscopic liver resection under hemihepatic vascular inflow occlusion using the lowering of hilar plate approach. Hepatobiliary Pancreat Dis Int 13:508–512. doi:10. 1016/S1499-3872(14)60293-9 Herman P, Kru¨ger J, Lupinacci R, Coelho F, Perini M (2013) Laparoscopic bisegmentectomy 6 and 7 using a Glissonian approach and a half-Pringle maneuver. Surg Endosc. doi:10.1007/ s00464-012-2681-x Rotellar F, Pardo F, Benito A, Martı´-Cruchaga P, Zozaya G, Pedano N (2012) A novel extra-glissonian approach for totally laparoscopic left hepatectomy. Surg Endosc. doi:10.1007/s00464012-2242-3 Hepp J, Couinaud C (1956) Approach to and use of the left hepatic duct in reparation of the common bile duct. Presse Med 64:947–948 Twaij A, Pucher PH, Sodergren MH, Gall T, Darzi A, Jiao LR (2014) Laparoscopic vs open approach to resection of hepatocellular carcinoma in patients with known cirrhosis: systematic review and meta-analysis. World J Gastroenterol 20:8274–8281. doi:10.3748/wjg.v20.i25.8274 Fuks D, Cauchy F, Fte´riche S, Nomi T, Schwarz L, Dokmak S, Scatton O, Fusco G, Belghiti J, Gayet B, Soubrane O (2015) Laparoscopy decreases pulmonary complications in patients undergoing major liver resection: a propensity score analysis. Ann Surg. doi:10.1097/SLA.0000000000001140 Siniscalchi A, Ercolani G, Tarozzi G, Gamberini L, Cipolat L, Pinna AD, Faenza S (2014) Laparoscopic versus open liver resection: differences in intraoperative and early postoperative outcome among cirrhotic patients with hepatocellular carcinoma—a retrospective observational study. HPB Surg. doi:10. 1155/2014/871251 Yamashita Y, Ikeda T, Kurihara T, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Kawanaka H, Shirabe K, Maehara Y (2014) Long-term favorable surgical results of laparoscopic hepatic resection for hepatocellular carcinoma in patients with cirrhosis: a single-center experience over a 10-year period. J Am Coll Surg 219(6):1117–1123. doi:10.1016/j.jamcollsurg.2014.09.003
123
24. Yoon S, Kim K, Jung D, Yu A, Lee S (2014) Oncological and surgical results of laparoscopic versus open liver resection for HCC less than 5 cm: case-matched analysis. Surg Endosc. doi:10. 1007/s00464-014-3980-1 25. Ahn KS, Kang KJ, Kim YH, Kim TS, Lim TJ (2014) A propensity score-matched case–control comparative study of laparoscopic and open liver resection for hepatocellular carcinoma. J Laparoendosc Adv Surg Tech A 24(12):872–877. doi:10. 1089/lap.2014.0273 26. Coles SR, Besselink MG, Serin KR, Alsaati H, Di Gioia P, Samim M, Pearce NW, Abu Hilal M (2015) Total laparoscopic management of lesions involving liver segment 7. Surg Endosc. doi:10.1007/s00464-014-4052-2 27. Xiang L, Xiao L, Li J, Chen J, Fan Y, Zheng S (2015) Safety and feasibility of laparoscopic hepatectomy for hepatocellular carcinoma in the posterosuperior liver segments. World J Surg. doi:10. 1007/s00268-015-2946-3 28. Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL (2003) Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 138:763–769 29. Figueras J, Lopez-Ben S, Llado L, Rafecas A, Torras J, Ramos E, Fabregat J, Jaurrieta E (2003) Hilar dissection versus the ‘‘glissonean’’ approach and stapling of the pedicle for major hepatectomies: a prospective, randomized trial. Ann Surg 238:111–119 30. Blumgart LH, Hann LE (2000) Surgical and radiologic anatomy of the liver and biliary tract. In: Blumgart LH, Fong Y (eds) Surgery of the liver and biliary tract, chap 1, 3rd edn. WB Saunders Co. Ltd., London, pp 21–22 31. Giordano M, Lopez-Ben S, Codina-Barreras A, Pardina B, Falgueras L, Torres-Bahi S, Albiol M, Castro E, Figueras J (2010) Extra-glissonian approach in liver resection. HPB (Oxford) 12:94–100 32. Tranchart H, Gaillard M, Chirica M, Ferretti S, Perlemuter G, Naveau S, Dagher I (2014) Multivariate analysis of risk factors for postoperative complications after laparoscopic liver resection. Surg Endosc. doi:10.1007/s00464-014-3965-0 33. Jiang G-Q, Chen P, Qian J-J, Yao J, Wang X-D, Jin S-J, Bai D-S (2014) Perioperative advantages of modified laparoscopic vs open splenectomy and azygoportal disconnection. World J Gastroenterol 20(27):9146–9153. doi:10.3748/wjg.v20.i27.9146 34. Muscari A, Collini A, Fabbri E, Giovagnoli M, Napoli C, Rossi V, Vizioli L, Bonfiglioli A, Magalotti D, Puddu GM, Zoli M (2014) Changes of liver enzymes and bilirubin during ischemic stroke: mechanisms and possible significance. BMC Neurol 14:122. doi:10.1186/1471-2377-14-122
