Autologous Blood Transfusion and Pringle Maneuver in Laparoscopic Segmental Hepatectomy for Benign Hepatic Neoplasms: A Retrospective Study

Abstract

Objectives:

To investigate the effect of autologous blood transfusion (ABT) and Pringle maneuver (PM) on postoperative early liver function and short-term postoperative results following laparoscopic liver resection in patients with benign hepatic neoplasms.

Materials and Methods:

We retrospectively analyzed the clinical data for 125 consecutive patients who underwent laparoscopic segmental hepatectomy from January 2015 to May 2018 (68 in the ABT group versus 57 in the PM group). We compared patients' characteristics and intra- and postoperative short-term outcomes between the groups.

Results:

The 2 groups were well matched regarding patients' clinical characteristics, types of liver resection, operative time, and histopathological findings (P > .05). Median blood loss was significantly lower in the PM group versus the ABT group (200 mL versus 750 mL, respectively; P < .01), and overall complication rates were similar (n = 12 [17%] versus n = 9 [16%], respectively; P > .05). The ABT group had significantly lower mean levels of total bilirubin, indirect bilirubin, aspartate transaminase, and alanine aminotransferase on postoperative days 1 and 3 (P < .05). The ABT group had a shorter hospital stay compared with the PM group (5.8 days versus 7.7 days, respectively; P < .05) and lower hospitalization costs (55,400 ± 15,400 versus 667,000 ± 21,600 CN dollars, respectively; P < .05).

Conclusions:

Compared with Pringle's maneuver, laparoscopic hepatectomy with ABT promoted early recovery of liver function and reduced hospitalization costs in select patients with benign hepatic neoplasms.

Introduction

Since the first laparoscopic liver resection was reported in 1992, several studies have suggested the feasibility, safety, aesthetic properties, and adequacy of laparoscopic hepatic procedures.^1–4 In addition, with technical standardization and advanced instrument development, the indications for laparoscopic hepatic procedures have expanded to include more complicated diseases, such as hepatocellular carcinoma and colorectal liver metastasis.^5,6 As a result, laparoscopic hepatectomy is now a standard procedure and is well accepted worldwide in modern liver surgery.

Pringle's maneuver, which is one method of hepatic inflow occlusion, has been widely used to control hemorrhage during liver resection.⁷ However, the superiority of Pringle's maneuver appears to be diminishing because both liver ischemia and reperfusion injury can be induced, and it is difficult to prevent tumor recurrence.^8–10 As an alternative method to control hemorrhage, selective hemihepatic vascular occlusion, which achieves vascular occlusion by manipulating the liver parenchyma or the hilar plate system, has the advantages of less blood loss and shorter operative time, as well as better recovery following liver resection,^11,12 Furthermore, as suggested by our previous clinical observations, laparoscopic hepatectomy without Pringle's maneuver may have less impact on recovery of liver function early postoperatively, especially in patients with an estimated blood loss volume of <1000 mL.

The duration of ischemia positively correlates with the severity of liver injury, and autologous blood transfusion (ABT) provides a balance between preventing severe blood loss and inducing liver damage. In this single-center study, we retrospectively evaluated the effect of ABT versus Pringle maneuver (PM) on recovery of liver function and perioperative outcomes following laparoscopic hepatectomy.

Materials and Methods

Between January 2015 and May 2018, data for 125 consecutive patients with benign hepatic neoplasms were considered for inclusion in this study. Inclusion criteria were as follows: no preoperative treatment and well-compensated chronic liver disease (Child–Pugh class A or B) without signs of severe cardiopulmonary or hepatorenal dysfunction. All patients underwent laparoscopic hepatectomy at our institution. We retrospectively analyzed patient's data from our clinical record database. Of the 125 laparoscopic liver resections, 68 procedures were performed without hepatic vascular inflow occlusion combined with autologous blood transfusion (the ABT group) and 57 procedures were performed using Pringle's maneuver (the PM group). We recorded patients' preoperative demographic parameters and imaging results as well as each patient's intraoperative parameters, including operative time, intraoperative blood loss, and the volume of ABT. We also recorded the following postoperative parameters: liver function tests and hemoglobin level on postoperative days 1 and 3, postoperative complications, postoperative hospital length of stay, and hospitalization costs.

All procedures were performed after obtaining informed patient consent, and all operations were performed by the same surgical team. This study was performed in accordance with the ethical guidelines of the 1975 Declaration of Helsinki and was approved by the Ethics Committee of our institution.

Definition of postoperative complications

Postoperative bleeding was defined as a postoperative bleeding volume exceeding 200 mL, with further bleeding expected, or the hemoglobin level was declined to <6 g/dL on postoperative days 0–3 after surgery. Biliary fistula was defined as an abnormal communication between the accessory biliary tract (gall bladder or cystic duct) and the gastrointestinal tract or main bile duct according to international criteria. Also, other complications included pulmonary infection, incision infection, and subphrenic abscess.

Surgical procedure

After appropriate preoperative preparation, patients were moved to the operating room for laparoscopic hepatectomy. Under general anesthesia, patients were positioned supine on the operating table with a footboard that allowed for 30° to 60° positioning in the reverse Trendelenburg position, and pneumoperitoneum was established by carbon dioxide insufflation at a pressure of 12 mmHg. All procedures were performed by seven experienced hepatobiliary surgeons during the study period. Four 5- to 12-mm trocars and a 45° laparoscope were inserted depending on the type of resection. Intraoperative ultrasonography was routinely used to confirm the location, size, and number of lesions and their relationships with major blood vessels. The resection line was marked using an ultrasonic dissector (Harmonic Scalpel; Ethicon Endo-Surgery, Cincinnati, OH) or a monopolar electrosurgical device (Peng's multifunction operative dissector). PM (total vascular inflow occlusion) or half-PM approach was selectively performed depending on tumor size, location, or portal vein involvement. After identifying and isolating the main root of the portal vein or its stems, an 8F catheter was placed around the duodenohepatic ligament (PM) or the portal vein stems (half-PM), respectively. Subsequently, tightening or loosening the hepatic vascular occlusion forceps or lock would cause the entire liver or body to clamp or unclamp if needed. In the ABT group, an 8F catheter was placed around the hepatoduodenal ligament or the portal vein stems to block hepatic portal flow during parenchymal transection when necessary. In the PM group, we encircled the hepatoduodenal ligament or the portal vein stems with the 8F catheter and applied a 15-minute clamping and 5-minute release protocol.

A disposable set for blood apheresis system (Haemonetics S.A. Signy-Centre, Switzerland) was prepared by anesthetists before operation, when the estimated blood loss was more than 500 mL. Blood from the trauma was collected through a tube, treated with anticoagulants and isotonic saline solution, and filtered into a cell saver unit during operation, and then the higher quality red blood cells were packaged in a collecting bag and ultimately reinfused into the patient.

We used both the ultrasonic dissector and the monopolar electrosurgical device as our main operative instruments during parenchymal transection. Minor bleeding was addressed by the ultrasonic dissector or the monopolar electrosurgical device; we controlled intraoperative severe hemorrhage from major blood vessels using titanium clips, vascular locks, or suturing using Prolene (Ethicon GmbH, Hamburg, Germany) suture. The specimen was extracted using an endoscopic retrieval bag through an expanded umbilical port incision, and an abdominal drainage tube was conventionally placed in all patients to detect hemorrhage or biliary fistula. Drains were removed on POD3–POD5 if additional criteria (the volume of daily peritoneal drainage fluid is <20 mL or abdominal ultrasound shows a fluid collection <3 cm on POD3) were met. Oral semiliquid foods were administered orally on POD2 according to the enhanced recovery after surgery criteria.

Statistical analysis

Descriptive statistics were expressed as number and percentage for categorical variables and as mean ± standard deviation for continuous variables. Differences between groups were evaluated using the Mann–Whitney U test for continuous variables. Fisher's exact test was used for categorical data. All statistical analyses were performed using the SPSS software package version 20.0 (IBM, Inc., Armonk, NY), and P < .05 was considered statistically significant.

Results

Patients' characteristics in each group are summarized in Table 1. A total of 125 patients with benign hepatic neoplasms underwent laparoscopic liver surgery (68 patients in the ABT group and 57 patients in the PM group). Both groups were well balanced regarding patients' demographics, clinical characteristics, excised liver segments, and histopathological findings (P > .05). Preoperative clinical and laboratory investigations were also comparable between the groups.

Table 1.

Patient Characteristics by Surgery Groups

Treatment group	ABT	PM	P
Number of patients, n	68	57	/
Age, years, mean ± standard deviation	46.5 ± 6.3	51.1 ± 9.1	NS
Gender ratio, F:M	38:30	31:26	NS
Child–Pugh class, A:B	61:7	52:5	NS
Hb, g/L	12.6 ± 1.2	12.9 ± 1.1	NS
TBil, μmol/L	19.5 ± 7.6	20.1 ± 5.3	NS
IBil, μmol/L	15.8 ± 5.9	16.2 ± 6.7	NS
AST, U/L	72.1 ± 14.5	76.1 ± 22.5	NS
ALT, U/L	35.2 ± 23.6	39.7 ± 20.5	NS
Segments
I	1	0	/
II/III	4	1	/
IV	5	4	/
V	14	11	/
VI	15	12	/
VII	11	12	/
VIII	5	4	/
Bisegments	13	15	/
Histopathology
Hemangioma	41	35	NS
Cystadenoma	10	7	NS
Hamartoma	5	3	NS
Others	13	12	NS

P < .05 has statistical significance.

ALT, glutamic-pyruvic transaminase; AST, glutamic oxalacetic transaminase; F, female; Hb, hemoglobin; IBil, indirect bilirubin; M, male; NS, not significant; TBil, total bilirubin.

Intraoperative and complication data are shown in Table 2. The operative time was longer (1.7 ± 0.3 hours versus 1.5 ± 0.4 hours) in the ABT group versus the PM group, respectively; however, the differences were not significant. The mean intraoperative blood loss volume in the ABT group was significantly higher compared with that in the PM group (750.0 ± 120.5 mL versus 200.5 ± 65.5 mL, respectively; P < .01). In the ABT group, the median volume of ABT was 500.0 ± 50.5 mL, while we did not perform ABT in the PM group. One patient underwent conversion to an open procedure secondary to uncontrollable bleeding in the ABT group, while 5 patients underwent conversion to PM. Comparing the ABT group with the PM group, the conversion rate was comparable between the 2 groups (1 versus 0, respectively; P > .05), and there were no statistically significant differences in the rate of complications between the 2 groups for bleeding (5.9% versus 5.3%, respectively; P > .05), biliary fistula (4.4% versus 3.5%, respectively; P > .05), or other complications (7.4% versus 7.0%, respectively; P > .05). In the ABT group, 6 patients experienced postoperative bleeding and were treated with hemostatics, while one patient underwent laparoscopic hemostasis for major bleeding in the PM group. Also, 5 and 4 patients in the ABT group and PM group developed fever and were treated with antibiotics only, respectively. Furthermore, in the ABT group, 2 patients developed biliary fistula (confirmed using ultrasonography or magnetic resonance imaging), which was successfully treated with drainage by placing a pigtail catheter percutaneously. Also in the ABT group, 1 patient underwent endoscopic retrograde cholangiopancreatography and stenting of the common bile duct.

Table 2.

Operative and Complication Data

Treatment group	ABT	PM	P
Operative time, hours	1.7 ± 0.3	1.5 ± 0.4	NS
Blood loss, mL	750.0 ± 120.5	200.5 ± 65.5	<.01^a
Volume of blood autotransfused, mL	500.0 ± 50.5	0	/
Conversion to open, n (%)	1 (1.5)	0	NS
Conversion to blocking, n (%)	5 (7.4)	/	/
Complications, n (%)
Bleeding	4 (5.9)	3 (5.3)	NS
Biliary fistula	3 (4.4)	2 (3.5)	NS
Others, n (%)	5 (7.4)	4 (7.0)	NS

Others including pulmonary infection, incision infection, and subphrenic abscess.

P < .05 has statistical significance.

NS, not significant.

Postoperative data are outlined in Table 3. The mean hemoglobin level was lower in the ABT group than that in the PM group on postoperative day 1 (11.3 ± 0.7 versus 11.9 ± 0.9 g/L, respectively; P > .05) and postoperative day 3 (11.6 ± 0.6 versus 12.1 ± 0.8 g/L, respectively; P > .05), although the differences were not significant (P > .05). The ABT group also had significantly lower total bilirubin, indirect bilirubin, aspartate transaminase, and alanine aminotransferase levels compared with the PM group on postoperative day 1 and postoperative day 3 (P < .05). The median length of hospital stay was 5.8 and 7.7 days in the ABT group and PM group, respectively (P < .05), and the mean hospitalization cost in the ABT group was 55,400 CN dollars versus 66,700 CN dollars in the PM group (P < .05).

Table 3.

Postoperative Data of Surgery Groups

Treatment group	ABT	PM	P
Hb (1 day), g/L	11.3 ± 0.7	11.9 ± 0.9	NS
TBil (1 day), μmol/L	21.5 ± 5.6	35.2 ± 7.1	<.05
IBil (1 day), μmol/L	17.1 ± 5.1	29.8 ± 6.7	<.05
AST (1 day), U/L	120.2 ± 56.2	239.8 ± 86.1	<.05
ALT (1 day), U/L	152.1 ± 35.3	348.7 ± 41.4	<.05
Hb (3 days), g/L	11.6 ± 0.6	12.1 ± 0.8	NS
TBil (3 days), μmol/L	19.5 ± 4.8	29.2 ± 7.5	<.05
IBil (3 days), μmol/L	16.8 ± 4.3	24.8 ± 5.1	<.05
AST (3 days), U/L	85.2 ± 29.2	169.2 ± 36.7	<.05
ALT (3 days), U/L	92.8 ± 25.7	238.5 ± 50.8	<.05
Hospital stay, days	5.8 ± 1.6	7.7 ± 2.1	<.05
Hospitalization expenses, RMB (1000)	55.4 ± 15.4	66.7 ± 21.6	<.05

Hb increase, Hb (postoperation) − Hb (preoperation).

P < .05 has statistical significance.

ALT, glutamic-pyruvic transaminase; AST, glutamic oxalacetic transaminase; Hb, hemoglobin; IBil, indirect bilirubin; TBil, total bilirubin.

Discussion

Laparoscopic hepatectomy generates relatively less peritoneal trauma and hemorrhage compared with conventional laparotomy, and may lead to decreased perioperative complications and duration of hospital stay.^13–15 Therefore, laparoscopic hepatectomy has gradually become a more standardized approach and is being performed worldwide commonly.¹⁶

Conventionally, Pringle's maneuver was performed to limit hemorrhage, but the technique can result in liver ischemia and reperfusion injury. Hepatic ischemia–reperfusion injury, as a leading cause of liver damage and even liver failure, is a serious concern and a major surgical challenge.^17,18 Moreover, warm ischemia–reperfusion injury not only impairs microvascular perfusion but also increases intrahepatic neutrophil infiltration and the risk of oxidative damage and induces hepatocyte apoptosis.^19,20 Compared with Pringle's maneuver, selective vascular occlusion benefits patients by decreasing hepatic damage and improving postoperative recovery of hepatic function, especially when excising tumors during hepatectomy.^8,21,22 Notwithstanding, selective vascular occlusion is a complicated and difficult procedure. Surgeons should have advanced experience in dissecting the porta hepatis to avoid further liver injury and have precise information regarding the position and size of the lesions. Despite these concerns, liver resections without Pringle's maneuver are associated with less damage to the residual liver and shorter hospital stays.^23,24 Animal models showed that rats not receiving Pringle's maneuver had better protection of liver function, better hemodynamic stability, and lower rates of microcirculatory failure.²⁵

Hemorrhage is associated with a higher rate of mortality following surgery²⁶ and is often managed with red blood cell transfusions, which is the preferred treatment to improve tissue perfusion and oxygenation in some clinical situations.²⁷ ABTs do not trigger an immune response and provide a higher quality red blood cell that has not been subjected to the adverse effects of blood storage and could be more cost-efficient than allogeneic blood transfusion when hypoperfusion occurs intraoperatively. Several randomized trials demonstrated that ABT represented a safe and effective treatment option for patients undergoing procedures with substantial anticipated perioperative blood loss.^28,29 Moreover, Nieder et al. believed that the risk of biochemical recurrence was not increased by transfusing salvaged blood during cancer surgery.³⁰ Thus, we carefully selected patients who received cell-salvaged blood and found no differences between our 2 surgical groups when comparing hemoglobin levels on postoperative days 1 and 3, which was what we expected.

ABT is a technique that may reduce ischemia–reperfusion injury by not blocking the portal blood supply and by including intraoperative ABT. It is well known that alanine aminotransferase and aspartate transaminase enzymes are common indicators to evaluate the degree of hepatocyte damage. Likewise, markedly increased transaminases may increase liver tissue damage and decrease blood supply to the liver remnant.²³ Our results showed that serum total bilirubin, indirect bilirubin, alanine aminotransferase, and aspartate transaminase levels on postoperative days 1 and 3 were significantly lower in the ABT group than those in the PM group. These results suggest that ABT might promote earlier recovery of liver function, as shown in previous studies.³¹ The comparison analysis in the present study showed no significant differences between the ABT and PM groups postoperatively regarding complication rates (17.7%. versus 15.8%, respectively), which was lower than that recorded by Tranchart et al.³² Compared with the PM group, the ABT group had a shorter hospital stay and lower hospitalization costs. Therefore, our results demonstrated that ABT was an efficient method regarding recovery of liver function and was associated with no short-term serious postoperative complications in patients requiring excision of benign hepatic neoplasms.

In our previous single-center study, two key conditions were required when performing ABT. The first was that intraoperative blood loss volume had to be <1000 mL. Once the loss of circulating blood volume reaches 20%, cardiovascular dysfunction and clinical decompensation occurs. Previous studies reported that compensatory adjustment mechanisms responding to shock cease with blood loss exceeding 1500 mL.³³ The second condition was that the tumor's distance to large vessels must be >10 mm when the lesion is adjacent to the right and middle hepatic veins; distances >10 mm increase the surgical difficulty and the risks of hemorrhage. In addition, we recommend against using ABT for hepatic malignant tumors because this approach may generate micrometastases that accelerate disease recurrence.³⁴

This study has several limitations. First, this was a retrospective analysis of a medical record database. Second, we did not use selective hepatic vascular exclusion in the present study because our team uses this technique most often for left/right hemihepatectomy or more complex liver excisions. Finally, the follow-up duration was comparatively short. High-quality, multicenter, large-sample randomized controlled trials, and long-term follow-up results are needed to precisely clarify the feasibility and superiority of ABT in laparoscopic hepatectomy for benign hepatic neoplasms.

Footnotes

Acknowledgments

We thank Jane Charbonneau, DVM, from Liwen Bianji, Edanz Group China for editing the English text of this article.

Authors' Contributions

J.Z. designed the scientific research designing and overall planning of the study. Q.Y. and X.W. improved the study procedures. L.J. and X.M. wrote the main article text and analyzed statistical data. Y.C., Q.Y., Z.W., and M.Q. prepared the tables.

Disclosure Statement

No competing financial interests exist.

Funding Information

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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