Abstract
Background Data and Objective:
Left lateral sectionectomy for liver transplantation in children performed through laparoscopy is an innovative procedure that was developed by considering our acquired experience in both laparoscopic liver resection and graft harvesting in living donors. The main goal was to minimize donor morbidity while preserving the abdominal wall. Herein, we report the technical feasibility and reproducibility, and compared it with open liver resection (OLR).
Methods:
Sixteen successive donors underwent a laparoscopic liver resection (LLR) from 2001 to 2005. They were compared with 14 other donors who underwent a standard open liver resection (OLR) during a first period (1998–2004). First, this report describes the technical features of laparoscopic resection. Second, perioperative morbidity and graft characteristics were compared according to the use or not of the laparoscopic approach.
Results:
Laparoscopic harvesting was successfully performed in 15 of 16 cases in an intention-to-treat basis. One conversion was required to ensure the quality of the laparoscopic repair of a left portal vein injury occurring during the pedicle dissection. No specific complication related to laparoscopy was observed. As compared with OLR, the operation was longer (320 ± 67 vs. 244 ± 55 minutes, P < 0.005). The blood loss was significantly lower in the LLR group (18.7 ± 44.2 vs. 199.2 ± 185.4 mL, P < 0.005). The morbidity rate was similar in both groups (18.7% in LLR vs. 35.7% in OLR). One donor in the LLR group experienced a bile leak treated by redo laparoscopy. Grafts were anatomically similar irrespective of the use of laparoscopy. The duration of hospital stay and use of self-infused morphine pump was not different between the 2 groups.
Conclusion:
Left lateral section harvesting by laparoscopy is a safe and reproducible procedure, allowing to obtain similar grafts as compared with laparotomy and can therefore be recommended to transplant centers that have previous experience in laparoscopic liver resection.
This study reports the technical feasibility and safety of laparoscopic left lateral sectionectomy in 16 living donors for pediatric liver transplantation. The results were compared with a case-control series of 14 open liver resections. The laparoscopic approach allowed obtaining similar grafts and morbidity as compared with laparotomy and can be recommended for left lateral section harvesting.
Living donor liver transplantation has become a widely accepted alternative to cadaveric transplantation in children. The use of liver grafts from living donors provides similar or even better short-term graft function and long-term survival rates, especially in children, as compared with whole and split cadaver liver grafts.1,2 The number of children receiving liver grafts from living donors is increasing annually in our institution. This procedure is, however, limited by surgical risks brought upon donors. Left lateral sectionectomy performed through open approach is a well-standardized procedure, associated with a lower rate of complications and mortality than right hepatectomy in living donors for adult transplantation. In living donations for liver transplantation in children, optimizing the postoperative course and limiting abdominal wall injury, especially in those young donors, remain of special concern. Minimally invasive donor nephrectomy using laparoscopic techniques has been widely reported and appeared beneficial for the donor as compared with standard open surgery, decreasing the overall morbidity, and improving donors' quality of life at low cost3–5 without deleterious effects on recipient's long-term kidney function.6
Considering our acquired expertise in laparoscopic liver resection7,8 and our training of standard open surgery as well as liver graft harvesting in living donors, we decided to propose laparoscopic left lateral sectionectomy in donors for liver transplantation in children. Since describing its technical feasibility with the first 2 cases,9 we have developed this procedure and we are now able to assess its safety and reproducibility in our center. Furthermore, during the first period of our experience in graft harvesting for children, a standard open surgical approach was used. This initial experience allowed us to compare both techniques of left lateral section harvesting. The primary goals of the present study were to validate the safety and reproducibility of the laparoscopic technique within our department of surgery.
PATIENTS AND METHODS
In 2002, we reported the feasibility of laparoscopic liver resection (LLR) in living donors for transplantation in children.9 Since these first 2 cases, 14 other donors consecutively underwent this procedure. Data obtained from these 16 donors (from 2001 to 2005) were compared with those obtained from 14 donors who underwent an open liver resection (OLR) during the first period of our experience in living donation (1998–2005). In case of emergency transplantation, the laparoscopic technique was not proposed for logistical reasons and the open approach was preferred.
Donor Assessment
All donors were the recipients' father or mother. All of them had a complete medical evaluation including social status, cardiovascular, pulmonary, and renal assessment. Besides usual blood tests and viral status, donors had screening for coagulation disorders. All were seen by a psychiatrist and interviewed in the Cochin department of clinical ethics (Dr. Veronique Fournier). Donor livers were evaluated by ultrasound, CT scan, and MRI including vascular mapping (portal, arterial, and hepatic vein reconstruction) and volume measurement. Arteriography, which was done during the first period, was no longer used to evaluate donor's vascular anatomy since 2000. Biliary imaging was performed using magnetic resonance cholangiography.
The laparoscopic technique was developed by 2 adult hepatobiliary teams (Cochin and Henri Mondor Hospitals) with extensive experience in open and laparoscopic liver resection and in liver transplantation of full and partial grafts. The grafts were harvested in Cochin Hospital and transplanted by a separate pediatric liver transplant team in Bicetre Hospital. Patients were informed of the innovative nature of the procedure and gave their written consent. This protocol has been approved by the Ethical Committee of Henri Mondor Hospital. All donors gave informed consent according to the French Law called “Bioéthique” (1994, modified in 2004) and the judge of Civilian Court recorded their consent.
Surgical Procedure
Since our first description of the laparoscopic technique,9 the procedure has been improved by both new devices and experience. Nonetheless, the operation was carried out according to the same steps irrespective of the use or nonuse of the laparoscopic approach. Two senior surgeons (O. Soubrane and D. Cherqui) performed this procedure, each one having expertise of both laparoscopic liver resection and graft harvesting in live donors. Both surgeons had previously performed a total of more than 150 laparoscopic liver resections, including major ones.
The liver graft included the left lateral section (ie, segments 2 and 3 according to Couinaud's classification), left branch of hepatic artery and left portal branch, left bile duct, and left hepatic vein. No clamping was used during parenchyma transection. Cholecystectomy and intraoperative cholangiography were not routinely performed.
The donor was in a supine position with his legs apart. Two monitors were placed over the left and right patient's shoulders. A carbon dioxide pneumoperitoneum was created and maintained at 11 mm Hg. Five trocars were inserted at sites shown in Figure 1. The middle trocar was placed 2 to 3 cm above the umbilicus to avoid any tangential vision to the whole left lateral section. These trocars did not require fascia incision (Versastep plus, Tyco Healthcare, Norwalk, CT). The liver was assessed visually with a 30° laparoscope. After this inspection, the left lateral section was mobilized by cutting its falciform and left triangular ligaments using harmonic scalpel (Ultracision, Ethicon Endosurgery, Cincinnati, OH) and monopolar scissors. The left hepatic artery(ies) and left portal vein were dissected free and taped (Fig. 2A). Arterial and portal branches assigned to the caudate lobe were clipped and divided (Fig. 2B) to increase the length of left hepatic artery and portal vein and facilitate their control. The liver transection was performed along the right side of the falciform ligament. The liver capsule and very superficial part of liver parenchyma were cut using a harmonic scalpel. Following, the liver transection was performed using an ultrasonic dissector (Dissectron, Satelec, Merignac, France). Hemostasis and biliostasis of small elements were performed using a bipolar electrocautery. Vascular elements larger than 2 mm, such as pedicles assigned to segment 4, were dissected using ultrasonic dissector and divided using clips or linear stapler (EndoGIA, Tyco Healthcare). When liver transection reached the hilar plate, the left hepatic bile duct was divided (Fig. 2C). Its distal end was closed with a 5/0 absorbable running suture or a clip. After completing the transection, the left hepatic vein was controlled and taped and the graft was thus ready for harvesting (Fig. 2 days). Following, an 8- to 10-cm suprapubic incision without muscular section was made. A 15-mm port was inserted allowing the introduction of a large specimen bag (Endocatch, Tyco Healthcare). The graft was harvested by clipping and dividing the arterial branch first. Its proximal part was locked in with bolt clip (Hem-O-Lock, Weck, Research Triangle Park, NC) while its distal end was clamped with a small bulldog clamp. Then a unilateral linear stapling device (EndoTA 30, Tyco Healthcare) was used to divide the portal and hepatic veins. The graft was put into the bag and extracted after completing the suprapubic fascia incision but always respecting the muscular integrity. The graft was then flushed with a 4°C UW solution through the left portal vein. Bile duct was washed out with UW solution as well.

FIGURE 1. Localization of the 5 port sites.

FIGURE 2. A, The left hepatic artery and left portal vein have been dissected free and taped. B, Dissection of a small portal branch assigned to segment 1. C, The left bile duct is cut. 2, The left lateral section is ready for harvesting.
The suprapubic incision was then closed and the pneumoperitoneum reinsufflated to check the quality of both hemostasis and biliostasis on the liver cut surface. Fascia was closed with absorbable sutures and cutaneous incisions were closed with subcuticular absorbable sutures. No drainage was used.
Postoperative Assessment
All complications were prospectively monitored since we began the laparoscopic technique. Usual biochemical liver tests were performed at postoperative days 1, 3, and 5. Postoperative clinical events and biologic tests were compared between the 2 groups according to the use or non use of laparoscopic approach (LLR vs. OLR). All patients in both groups normally received morphine (patient-controlled analgesia). After discharge, all donors were followed up and seen on postoperative months 1, 3, and 12 with biochemical liver tests and ultrasound.
Statistical Analysis
Quantitative variables were compared using the Mann-Whitney U test. Qualitative variables were analyzed using the χ2 test or Fisher exact test where appropriate. Data of quantitative variables were expressed as mean ± SD or as median and range. Differences at P less than 0.05 were considered significant.
RESULTS
Donor Characteristics
The preoperative donor's and graft's characteristics are given in Table 1. There was no statistical difference between the 2 groups (LLR and OLR).
TABLE 1. Preoperative Characteristics of Donors Who Underwent Left Lateral Sectionectomy Under Either Laparoscopy or Laparotomy

Surgical Features
Overall, the complete laparoscopic graft harvesting was successfully performed in 93% of cases in an intention-to-treat basis. The fourth laparoscopic approach was converted to laparotomy. In this case, a left portal branch injury occurred during the hilar plate section. The vessel was closed by stitches under laparoscopy without significant blood loss. However, we decided to convert to laparotomy to make sure that no stenosis would occur. The liver graft was successfully transplanted with normal subsequent liver function.
No gas embolism or hemorrhage occurred. Bleeding was nil in 80% of the patients who underwent laparoscopic resection, and ranged from 0 to 150 mL in the whole group. As compared with laparotomy, the laparoscopic approach was associated with significantly less blood loss volume (18.7 ± 44.2 mL vs. 199.2 ± 185.4 mL, P < 0.005). No patient was transfused in either group.
The use of the laparoscopic technique significantly increased the operative time (320 ± 67 minutes vs. 244 ± 55 minutes, P < 0.005). However, operation time in the laparoscopic group decreased from the first to the last case (Fig. 3) and was reduced by about 1 hour.

FIGURE 3. Evolution of the operative time since the beginning of the series. Case 4 required conversion to laparotomy.
Postoperative Outcome
No patients died. The overall morbidity in case of laparoscopic approach was 18.7%. One patient in the laparoscopy group required reoperation because of a bile leak coming from the hilar plate (segment 1 duct) and was closed with a 5/0 absorbable suture through redo laparoscopy. During this second operation, a cholecystectomy and a cholangiography were performed showing a normal right cholangiogram and biliary confluence. The postoperative course was uneventful and the patient was well after 12 months of follow-up (normal liver tests and ultrasonography). The morbidity rate was 35.7% in the OLR group (not significant). Complications are detailed in Table 2. In the laparoscopy group, the 2 wound hematomas occurred on the suparapubic incision and were not related to trocar insertion.
TABLE 2. Donor's Postoperative Complications Occurring After Left Lateral Sectionectomy Performed Through Either Laparoscopy or Laparotomy

The mean length of hospital stay was 7.5 ± 2.3 days (range, 5–16 days) and 8.1 ± 3.0 days (range, 6–10 days) in LLR and OLR group, respectively (not significant). The mean duration of venous infusion (3.7 ± 1.2 vs. 3.9 ± 1.3 days, respectively) and use of self-infused morphine pump (2.0 ± 0.9 vs. 2.2 ± 0.9 days, respectively) were not different between the LLR and OLR groups. Results of the laboratory tests, summarized in Table 3, were not different between the 2 groups.
TABLE 3. Biological Data Before and After Left Lateral Sectionectomy in 30 Living Donors

Donors Follow-up
No donors were rehospitalized after discharge. They were seen as outpatients on postoperative months 1, 3, and 12. All donors returned to work within 2 months after surgery. In the laparoscopy group, the median follow-up was 15 months (range, 1–51 months) and 10 of 16 donors have reached 1 year of follow-up at the time of the study analysis. All had normal physical examination and their liver biochemical tests were within normal values. Ultrasound of the remnant liver was normal in those 10 patients with homogenous parenchyma, patent portal vein, normal resistance index of the hepatic artery, and no bile duct dilatation. Follow-up liver biochemical tests of donors from the laparoscopy group are given in Table 4.
TABLE 4. Donor's Biological Data 1 and 12 Months After Laparoscopic Left Lateral Sectionectomy

Liver Grafts and Recipients Outcome
The median warm ischemia time was 10 minutes (range, 6–12 minutes) in the LLR group, longer than those observed in the OLR group: 5 minutes (range, 2–7 minutes) but not significantly. Overall, liver grafts obtained either by laparoscopic or open approach were anatomically similar. The mean number of harvested left arteries and bile ducts were similar in both groups. Most of the grafts (80%) had a single left hepatic duct in case of laparoscopic harvesting and were comparable to those obtained by laparotomy (70%). Anatomic characteristics of the liver grafts are shown in Table 5.
TABLE 5. Characteristics of the Left Lateral Section Grafts

All liver grafts were successfully transplanted. Two children recipients died, 1 in each group. In the laparoscopy group, 1 recipient died on postoperative day 7 from sepsis and multiorgan failure. In the laparotomy group, 1 recipient died on postoperative day 25 from septic shock after subsequent kidney transplant. Two children recipients have been retransplanted, 1 in each group, because of recurrent fulminant autoimmune hepatitis (OLR group) and liver graft necrosis due to portal vein thrombosis (LLR group). Surgical complications, shown in Table 6, were not different between the 2 groups. In the LLR group, 15 of 16 children recipients were alive after a median follow-up of 15 months (range, 1–51 months). In the OLR group, 13 of 14 children recipients were alive after a median follow-up of 47 months (range, 4–78 months).
TABLE 6. Surgical Complications in Children Recipients According to the Technique of Liver Graft Harvesting

DISCUSSION
This study reports the first documented and comparative experience of a left lateral sectionectomy performed by laparoscopy in living donors for liver transplantation in children. However, to recommend this technical innovation, its safety and reproducibility as well must be demonstrated. The minimal experience required to achieve this challenging procedure includes both laparoscopic liver resection and graft harvesting in living donors. Although 2 experienced surgeons in both areas decided to collaborate, this procedure also took benefit from new devices and instrumentations, especially modern transection tools and reliable vascular staplers. Harvesting of the left lateral section in living donors probably represents one of the more relevant uses of the laparoscopic approach to liver resection, consisting in exclusive resection without reconstruction, and preserving the abdominal wall in young and healthy donors. However, the theoretical advantages for the donor must be carefully studied and balanced with the unknown effects in the recipients.
Although we have demonstrated the feasibility and reproducibility of this technique, several rules remain mandatory. This procedure was in fact divided into 2 steps; the first one included the pedicle dissection with control and taping of vascular elements while the second one consisted of bile duct section and parenchyma transection. These 2 steps were shared and performed in “crop” rotation between the 2 senior surgeons: they performed alternatively the pedicle dissection and the parenchyma transection. This shared responsibility between 2 senior surgeons was chosen to warrant a high level of safety in any technical gesture during the whole procedure.
For the laparoscopic technique, we wanted to strictly use the same principles of open liver resection. That is why we used an ultrasound dissector to carefully isolate any vessel and bile duct one by one. Then, hemostasis and biliostasis were done with bipolar coagulation or bolt clips. We never used “en masse” or blind stapling of liver parenchyma. A left portal vein injury occurred in the laparoscopic group during the fourth procedure, while cutting the left bile duct and hilar plate. However, this vessel injury did not lead to any significant bleeding and was closed immediately by stitches. Conversion to laparotomy was decided as a principle to avoid any risk for liver graft vascularization. At laparotomy, the left portal vein was patent and would have allowed us to complete surgery through laparoscopy. The second surgical complication in the LLR group was a bile leak due to a small bile duct arising from segment 1. We do not consider this complication as directly related to the laparoscopic technique since bile leak is a well-known complication of open liver resection as well.10 A previous case-control study from one of us has demonstrated that laparoscopic left lateral sectionectomy was associated with decreased blood loss when compared with standard open resection.8 The present results are consistent with those reported by Lesurtel et al.8 Although the donors in the open surgery group underwent hepatectomy during the first period of the donation program, in other words, during a less experienced period, there are several reasons that might explain the decreased blood loss associated with laparoscopic resection: first, the transection meticulously performed with systematic coagulation of millimeter vessels; second, the positive role of pneumoperitoneum tamponing the cut surface; and finally, our acquired knowledge of liver resection performed without pedicle clamping.11 We also confirmed a longer operation when performed through the laparoscopic approach as compared with open resection. The duration of the procedure has decreased from the first to the last case reflecting the learning curve. Indeed, decreasing the operating time is not a crucial goal to achieve in this indication. On the other hand, limiting the warm ischemia time is more important, and we have demonstrated that laparoscopy did not impair the duration of graft extraction.
In various laparoscopic operations including liver resections and nephrectomy in live donors, several reports have advocated the use of the hand-assisted technique.12,13 One major goal of our laparoscopic left lateral sectionectomy was to minimize the abdominal wall injury in young healthy donors. That is why we did not use the hand-assisted technique through a midline or subcostal incision which, to us, might considerably diminish the benefit of the technique. At last, using the suprapubic incision was not consistent with a remote operative site for hand insertion.
The left lateral section is a favorable anatomic entity for laparoscopic resection because of its anterior position and of a limited number of anatomic variations.14 However, our main technical problem was the ability to cut the left bile duct at the adequate level. Modern preoperative assessment, especially MRI biliary reconstruction, is one of the key points to achieve this goal.
The technique of laparoscopic nephrectomy in living donors, first described in 1995,15 has largely spread and is now performed in many centers all around the world. The use of this technique has led to a decreased morbidity rate, a decreased postoperative pain, a shorter hospital stay, a lower coast, a better quality of life, a faster return to work, and an increase in donation rates.16–18 In our study, we did not show any difference between LLR and OLR regarding the duration of hospital stay and morphine use. However, it is still a short series that was undertaken as a phase 1 or 2 clinical trial to demonstrate the safety and reproducibility of the technique. Theoretical advantages about the time to rehabilitation, quality of life, decreases in morbidity rates, and increases in donation rates remain to be eventually established. Moreover, the duration of hospital stay and time to return to work might be difficult to analyze precisely and to compare between different countries. In France, for example, surgical treatment is free of charge and the social security provides full financial support to compensate salary loss, especially in living donors. Thus, in France, the donors often prefer to stay at the hospital until they feel they have fully recovered from surgery.
Results of liver transplantation in children are still under evaluation but did not show adverse effects of laparoscopic resection upon recipient's mortality and morbidity. These results should be compared with those observed after the open standard resection in a larger series. Liver graft outcome appears to be a key point in the future because the results of kidney transplantation in young children recipients showed an increase in delayed graft function and acute rejection rates when the renal graft was harvested through laparoscopy.19 The reasons that might explain this impairment in renal function are unclear, but the pneumoperitoneum necessary to perform laparoscopy might be associated with hemodynamic disturbance in the kidney vasculature. In our study, anatomic characteristics and warm ischemia time were not different between the 2 groups. Extraction of the graft through the suprapubic incision in a bag did not lead to specific problem, especially graft injury. Yet, the effect of prolonged carbon dioxide pneumoperitoneum on liver graft function remains unknown.
CONCLUSION
The left lateral sectionectomy performed through a laparoscopic approach is a safe procedure that can be performed repeatedly in our center, allowing to decrease intraoperative blood loss and obtain similar grafts and similar results in both donors and recipients as compared with laparotomy. Since the donor's abdominal wall is preserved, we consider that the laparoscopic approach might be the technique of choice for left lateral sectionectomy. The impact on morbidity and quality of life in a larger series of donors, as well as the long-term results in child recipients need further evaluation.
ACKNOWLEDGMENTS
The authors thank Ms. Nancy Farrell and Mr. William Cooper for their expert assistance in preparing this manuscript.
Footnotes
Reprints: Olivier Soubrane, MD, Service de Chirurgie, Hôpital Cochin, Assistance Publique–Hôpitaux de Paris, Université Paris-Descartes, 27 rue du Faubourg St. Jacques, 75014 Paris, France. E-mail: olivier.soubrane@cch.aphp.fr.
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