Laparoscopic liver resection: a review.

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Journal of Visceral Surgery (2013) xxx, xxx—xxx

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REVIEW

Laparoscopic liver resection: A review H. Tranchart a,b,∗, I. Dagher a,b a

Service de chirurgie viscérale minimale invasive, hôpital Antoine-Béclère, AP—HP, 157, rue de la Porte-de-Trivaux, 92140 Clamart, France b Université Paris-Sud, 91405 Orsay, France

KEYWORDS Hepatectomy; Laparoscopy

Summary Laparoscopic liver surgery was slower to develop than other fields of laparoscopic surgery because of a steep learning curve, and fear of uncontrolled bleeding or gas embolism. However, laparoscopic liver resection (LLR) is associated with significant advantages: faster recovery, less post-operative pain, less morbidity, easier subsequent surgery and better cosmetic results. Since the inception of this technique, more than 3000 procedures have been reported. The aim of this update was to review the literature in order to define the indications (malignant tumors, benign tumors, major resections), the advantages and limits of this approach as well as the expected value of new technology, such as intra-operative guidance or robotics, in the development of this branch of surgery. © 2013 Elsevier Masson SAS. All rights reserved.

Introduction The first laparoscopic liver resection (LLR) was reported by Gagner at al. in 1992 [1]. Unlike other domains in laparoscopic surgery, hepatic surgery was very slow to develop. The reputed obstacles to this approach included foremost a steep learning curve, as well as the need to develop familiarity with laparoscopic equipment, learning how to mobilize the liver and the techniques of parenchymal transection, fear of difficult-tocontrol bleeding or gas embolism, and issues regarding patient-selection. However, in spite of these difficulties, LLR has invaluable potential advantages including minimal parietal violation (quicker return to normal activities [2], decreased peri-operative pain [3] and improved cosmetic result), decreased morbidity (reduced blood loss and need for transfusion [4], less post-operative ascites in cirrhotics [4,5], fewer pulmonary complications [4]), and simplification of subsequent surgery (iterative hepatectomy [6], hepatic transplantation [7]). Since the inception of these techniques, more than 3000 procedures have been reported [8]. Initial experiences involved benign lesions [9] but

∗ Corresponding author. Service de chirurgie viscérale minimale invasive, hôpital Antoine-Béclère, AP—HP, 157, rue de la Porte-de-Trivaux, 92140 Clamart, France. E-mail address: [email protected] (H. Tranchart).

1878-7886/$ — see front matter © 2013 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.jviscsurg.2013.10.003

Please cite this article in press as: Tranchart H, Dagher I. Laparoscopic liver resection: A review. Journal of Visceral Surgery (2013), http://dx.doi.org/10.1016/j.jviscsurg.2013.10.003

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H. Tranchart, I. Dagher

in recent years, series of more than 100 resections for malignant tumors have been reported [10]. Left lobectomy is probably the simplest LLR and is presently standardized by certain authors [11]. Several experienced groups have performed major hepatic resections after strict patient selection [12,13], even though this technique remains difficult. There are still no randomized trials comparing laparoscopy versus laparotomy approaches to hepatic resections. A prospective trial is underway in spite of predictable problems regarding inclusion criteria [14]. The goal of this review was to define the indications, the advantages and the limits of this surgical approach based on reports in the literature and also to analyze the potential value of new technologies, such as intra-operative guidance or robotics. The information in this review was extracted from the literature after a Medline search.

Patient selection There are presently no formalized indications for LLR. A consensus of experts who met in Louisville, Kentucky, USA in 2008, said the best indications for this technique were solitary lesions, less than 5 cm, located in the anterior segments, at a distance from the line of transection, the hepatic hilum, and the vena cava [15]. Experienced centers, however, perform LLR for tumors in the posterior segments (I, VII and VIII) or central liver, bilobar resections, or resections close to the vena cava or hepatic pedicle [16,17]. Ever since this consensus conference took place, surgical indications have continued to evolve and tumors greater than 5 cm are no longer considered by certain teams as a contraindication to laparoscopic surgery; close proximity to the portal pedicle has also become a debatable limit as laparoscopic magnification allows very precise extrahepatic portal dissection [18]. In our center, the other selection criteria for laparoscopy include an American Society of Anesthesiologists (ASA) score ≤ 3, a non-cirrhotic liver, or compensated cirrhosis (esophageal varices ≤ grade 1 and platelet count ≥ 80 × 109/L). We do not consider patient weight a contra-indication, and, in fact, we prefer this approach in overweight patients. The body mass index (BMI) of patients undergoing right liver resections in our unit is 20.7 kg/m2 (20.4—46.3 kg/m2 ). Previous upper abdominal surgery is not a contra-indication and in our experience, this concerns 22% of patients, 5% of whom had already undergone hepatic surgery (unpublished data).

Major and minor hepatectomies Tumorectomies or solitary segmentectomies seem to be best suited to the laparoscopic approach, allowing hepatic parenchymal sparing and allowing the dissection plane to remain distant from the major vessels. Paradoxically, these resections are probably the most difficult and require previous experience in minor anatomic LLR (left lobectomy) [17]. We recently reported our experience comparing anatomic LLR (hepatectomy, left lobectomy and right hepatectomy: performed in our unit after initial control and division of the vessels supplying the resected liver) to LLR performed with selective vascular control (atypical resections, solitary or multiple segmentectomies) [18]. Blood loss did not differ between the two groups, despite the larger hepatic volume resected in the anatomic resection group. Operative

time was greater for atypical hepatectomy and segmentectomy; a possible explanation is the time required for hepatic parenchymal transsection. During atypical resections, parenchymal dissection is performed in different planes, making the view of the hepatic section more difficult to see, especially by laparoscopy. A sagittal, antero-posterior approach is used to divide the liver during left lobectomy and left and right hepatectomies, which facilitates the operation by direct control of the vessels that are always located in an horizontal plane. Left lobectomy appears best adapted to laparoscopic hepatic surgery. In 2009, six centers (3 European, 2 American and one Australian) reported 210 major LLR performed over a period of 10 years [12] i.e. approximately four major LLR per year and per center. Median duration of operation was 250 minutes (90—655 min) with median blood loss of 300 mL (20—2500 mL). The conversion rate was 12.4%. Complete clamping of the hepatic pedicle was necessary in 11.4% of patients. Two deaths occurred post-operatively (one due to pulmonary embolism on day 10 and one from sepsis originating from urinary tract infection one month postoperatively). Specific and non-specific morbidity were 8.1% and 13.8%, respectively. Median duration of hospital stay was six days (1—34 days). The authors compared their recent experience to their initial experience (first 15 patients in each center): duration of operation, blood loss, hepatic pedicle clamping, conversion rate and length of stay all improved significantly in the second part of their experience. Ten European centers recently reported their experience with LLR over a 15-year period [19]. Of 2245 LLR, 495 (22%) were major resections. Two centers used a ‘‘hand-assisted’’ technique with one hand in the abdomen. The conversion rate was 10.8%. Mean blood loss after right and left hepatectomy was 437 mL and 275 mL, respectively. Three retrospective comparative studies focusing on major LLR have been published (Table 1) [2,20,21]. The study by Abu Hilal at al. [20] compared right hepatectomy via laparoscopy (n = 36) or via laparotomy (n = 34). Duration of operation was significantly longer via laparoscopy. The conversion rate was 11%. There was no significant difference in terms of morbidity or resection margins between the two groups. Hospital stay was significantly shorter in LLR. According to our experience, the type of hepatic resection should not be determined by the approach but rather by the type of lesion and the underlying parenchymal status. For example, a lesion in segment VIII should not be removed by right hepatectomy just because the laparoscopic approach is easier than that for laparoscopic segment VIII resection. If this segmentectomy seems difficult via laparoscopy, it is preferable to perform it via laparotomy in order to maximize parenchymal sparing; this outweighs the choice of the surgical approach in the short term, and also, sometimes, in the long term.

Malignant and benign tumors The carcinologic efficacy of LLR was much debated at first. Many surgeons were unenthusiastic because of fear of margin involvement and trocar orifice tumor seeding discouraged. Since then, several retrospective studies have shown that surgical margins were equivalent and that survival was comparable irrespective of whether the operation was performed via laparoscopy or laparotomy [4,22].


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Abu Hilal et al., 2011 [20] Dagher et al., 2009 [2] Cai et al., 2009 [21]

Number of laparoscopies

36 22 19

Conversion rate, %

11 9 10.5

Duration of operation, min

Morbidity, %

Length of stay days

Laparoscopy

Laparotomy

P

Laparoscopy

Laparotomy

P

Laparoscopy

Laparotomy

P

300 360 222

180 328 204

< 0.0001 0,07 0.516

14 9 11

15 34 21

0.9 0.04 0.66

5 8.2 9

9 12.5 13

< 0.0001 0,009 0,086

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Intra- and post-operative results after major liver resections via laparoscopy or laparotomy in retrospective comparative studies.

Authors, date


Laparoscopic liver resection: A review


Table 1

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However, there are no prospective studies in laparoscopic surgery to confirm these oncologic results. Moreover, to the best of our knowledge, no instances of trocar site metastasis have been reported for LLR in the setting of malignant tumor. Patients with hepatocellular carcinoma (HCC) are potential candidates for LLR [23]. In our experience, 27% of patients with HCC who are candidates for resection can be operated via laparoscopy [4]. The advantages of this approach in this setting are less intra-operative bleeding, lower rate of edema and/or ascitic decompensation (by preservation of abdominal wall portocaval venous collateral circulation) and less post-operative adhesions, which facilitates eventual secondary hepatic transplantation. Only eighteen retrospective comparative studies of patients undergoing operation for HCC are available in the literature (Table 2) [4,5,22,24—38]. Overall and disease-free survival after laparoscopy and laparotomy were comparable in all these studies. A larger comparative study by Ker at al. [34] reported less blood loss (138 vs. 1147 mL; P < 0.001) and risk of transfusion (7% vs. 51%; P < 0.001) with LLR. Morbidity was lower with LLR (6% vs. 21%; P < 0.001). Another matchedpair comparative study, published by our team [4], showed the same results and reported a lower rate of edematoascitic decompensation after LLR (7.1% vs. 26.1%; P = 0.03). Laurent at al. [7] reported 24 patients who had undergone salvage transplantation after hepatectomy for HCC. Half of these patients had initially undergone laparotomy, and the other half laparoscopy. During transplantation, the operative time required for the hepatectomy stage and for the entire procedure was significantly shorter in patients who were initially operated via laparoscopy (2.5 vs. 6.2 h and 4.5 vs. 8.3 h, respectively; P < 0.05), blood loss was also lower (1200 vs. 2300 mL; P < 0.05). As patients who underwent LLR were obviously highly selected, case-matching is difficult and therefore, also, so is the interpretation of results from available studies. Liver colorectal metastases (LCRM) may be accessible to laparoscopic resection [39]. Management of these patients often requires multiple hepatic resections and laparoscopy simplifies subsequent operations. In the literature, only six retrospective comparative studies on patients undergoing LCRM are available (Table 3) [40—45]. The largest study published to date by Castaing at al. [40] involved only purely laparoscopic hepatic resection. Two groups of 60 patients undergoing either laparoscopy or open laparotomy were compared. The rate of transfusion was lower in laparoscopy (15% vs. 36%; P = 0.007). Post-operative morbidity and survival were comparable between the two groups. Here again, patient selection in anticipation of the laparoscopic approach makes matching and therefore interpretation of results difficult. The benefits of simultaneous laparoscopic resection of a colorectal primary tumor and liver metastases remains under debate. The theoretical advantages of this approach are the same as those for any laparoscopic approach and are also related to the facility with which repeat hepatectomy can be performed in patients at high risk of liver recurrence. Two comparative studies are available [42,43]. The study by Huh at al. [43] involved two groups of 20 patients who underwent combined resection via either laparoscopy or laparotomy. No mortality was reported in either group, and no conversions were necessary. Blood loss was less in the laparoscopy group (350 vs. 500 mL; P = 0.048). Operative time was greater for the laparoscopic group (358 vs. 278 min; P = 0.004). Post-operative

morbidity and survival were comparable between the two groups. There are few data available on the specific treatment of cholangiocarcinoma via laparoscopy. In selected cases, peripheral intrahepatic cholangiocarcinoma can probably be treated via laparoscopy, much like metastases or HCC. Management of hilar cholangiocarcinoma is more problematic. The risk of vascular involvement, the difficulty in biliary reconstruction and the necessity for high quality lymphadenectomy limit the possibility of a laparoscopic approach. Gumbs at al. [46] recently reported a series of 14 patients undergoing laparoscopic resection for intra (n = 9) or extrahepatic (n = 5) cholangiocarcinoma. The mean blood loss was 233 mL (100—400 mL) and 240 m (0—400 mL), respectively. The conversion rates were 11% and 20%, respectively. This series also included 15 patients with gallbladder carcinoma. R0 resections were obtained in all patients. The conversion rate was 7% and blood loss was 160 mL (0—400 mL). Lymphadenectomy harvested an average of four (1—11) lymph nodes. The other available studies all included fewer than 20 patients [47]. Very few series have been dedicated to the surgical management of benign tumors (adenoma, angioma, focal nodular hyperplasia or biliary cysts [48,49]). The development of laparoscopy has pushed certain teams toward a more aggressive surgical approach to these lesions [50]. From a theoretical view point, laparoscopy is associated with decreased intra- and post-operative morbidity and is particularly suited to surgical management in this frequently young population [9]. The decision whether or not to operate must be based on the symptomatic character of the lesion (which is sometimes difficult to prove) or, for certain adenomas, on the risk of malignant degeneration or bleeding. Of note, the expert panel in the 2008 consensus conference [15] concluded that unroofing of a cyst via laparoscopy was not, properly speaking, a hepatic resection, and should not be considered as such. Abu Hilal at al. [48] reviewed the patient records of 46 patients who underwent LLR for benign tumors (28% of which were major resections). The diagnosis was uncertain preoperatively in 11 patients (for which the final diagnosis was HCC in one). Whereas pre-operative imaging arrives at the correct diagnosis in more than 95% of cases, this diagnostic uncertainty rate of 24% (11/46) can be imputed to a lack of radiologic experience or to excessive operative indications. However, the immediate results were good with post-operative morbidity at 7%, zero mortality, and a median hospital stay of 4 and 3 days, respectively, after major and minor resection.

Limits of the laparoscopic approach Laparoscopic hepatic surgery also has its limits. Manual palpation is not possible, except in the case of intra-abdominal hand-assisted LLR. The tactile sensation transmitted through laparoscopic graspers is limited. Intraoperative sonography in the hands of certain teams has been said to compensate for the inability to palpate the tumor. Intra-operative sonography is performed routinely in hepatic surgery, in search of undiagnosed additional lesions, and is also important in laparoscopy to guide the operative procedure. A recent comparative study showed that sensitivity and specificity of intra-operative sonography were equivalent, whether performed via laparoscopy or laparotomy [51].


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Table 2 Overall survival and recurrence-free survival after liver resection for hepatocellular carcinoma, via laparoscopy or laparotomy in retrospective comparative studies. Authors, date

Cheung et al., 2013 [37] Kanazawa et al., 2013 [38] Lee et al., 2011 [32] Ker et al., 2011 [34] Hu et al., 2011 [33] Kim et al., 2011 [35] Truant et al., 2011 [36] Tranchart et al., 2010 [4] Aldrighetti et al., 2010 [31] Belli et al., 2009 [24] Lai et al., 2009 [25] Endo et al., 2009 [27] Sarpel et al., 2009 [22] Belli et al., 2007 [30] Kaneko et al., 2005 [28] Lee et al., 2007 [26] Laurent et al., 2003 [5] Shimada et al., 2001 [29]

Number of laparoscopies

32 28 33 116 30 26 36 46 16 67 60 57 20 23 61 25 13 50

Overall survival at 1, 2*, 3** or 5*** years, %

Recurrence-free survival at 1, 2*, 3** or 5*** years, %

Laparoscopy

Laparotomy

P

Laparoscopy

Laparotomy

P

76.6*** — 81.8** 62.2*** 50*** — 70*** 74.4** — 67** 60** — — 86* — — 89** —

57*** — 80.6** 71.8*** 53.3*** — 46*** 73** — — — — — 82* — — 55** —

0.1 — ns ns ns — 0.07 ns ns ns ns ns ns ns ns ns 0.04 ns

54.5*** — 51** — — 84.6* 35.5 60.9** — 52** 52** — — — — — 46** —

44.3*** — 55.9** — — 82.8* 33.6 54.3** — — — — — — — — 44** —

0.08 — ns — — ns ns ns ns ns ns ns ns — ns ns ns ns

ns: non significant.

More than 75% of LLR reported to date have been purely laparoscopic procedures [8]. However, some surgeons prefer hand-assisted LLR to allow manual guidance of the operative procedure. The technique of hand-assisted LLR, however, cannot be considered to increase the safety of the operation because, in fact, it decreases the visibility of the operative field. Notwithstanding, this technique is the most widely reported technique for major hepatectomies on living-donors [52]. Fear of uncontrollable major bleeding remains a barrier to the development of the laparoscopic approach. Nonetheless, there have not been any intra-operative deaths reported in the largest study on major LLR [12]. Of the 26 conversions to laparotomy, six cases (23.1%) were related to persistent moderate bleeding during parenchymal division while three conversions were required for bleeding from a portal vein branch injury, a hepatic vein injury and a vena cava injury, respectively. In all cases, bleeding was controlled during laparoscopy and the conversion was performed without any vital compromise. In our experience, the

risk of bleeding has not been a limiting factor to development of this approach. However, increased morbidity and mortality related to poorly controlled bleeding or bleeding controlled only after significant blood loss has not been clearly defined in the literature. At the present time, laparoscopic vascular reconstruction is difficult. The risk of gas embolism has haunted surgeons ever since the inception of laparoscopic liver surgery. When anesthesia is performed maintaining a low central venous pressure (CVP) during LLR, there is a theoretical increased risk of CO2 embolism due the pressure gradient with the insufflation pressure exceeding the CVP. Frequent embolisms of CO2 from the pneumo-peritoneum have been shown to occur [53]. These embolisms, however, are without any clinical repercussion, as shown in animal [54] as well as human [55] studies. Bleeding from the liver transection surface depends on the balance between the portal affluent and arterial supply, on one hand, and on the pressure in the suprahepatic venous network, on the other (minimized by a low CVP and the counterpressure from the pneumo-peritoneum). Positive

Table 3 Overall survival and recurrence-free survival after liver resection for colorectal metastases, via laparoscopy or laparotomy in retrospective comparative studies. Authors, date

Cannon et al., 2012 [44] Cheung et al., 2012 [45] Huh et al., 2011 [42] Castaing et al., 2009 [40]

Number of laparoscopic operations

35 20 20 60

Overall survival at 1, 2*, 3** or 5*** years, %

Recurrence-free survival at 1, 2*, 3** or 5*** years, %

Laparoscopy

Laparotomy

P

Laparoscopy

Laparotomy

P

36*** — 52.8** 82**

42*** — 61** 70**

ns 0.2 ns ns

15*** — — 47**

22*** — — 40**

ns 0.3 — ns

ns: non significant.


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pressure for pneumo-peritoneum has proven its efficacy in decreasing bleeding in the liver trauma animal model [56]. The intra-abdominal pressure setting used during LLR is generally between 10 and 12 mmHg and can be increased to 15 mmHg in case of significant bleeding from the surface of the hepatic transection [18]. In our experience, limited temporary increase in pneumo-peritoneum pressure allows good control of bleeding of parenchymal bleeding and has never resulted in any untoward effect to the patient [18]. However, this technique is not applicable to large hepatic vein injuries, and particular caution is warranted during the dissection of these structures. The posterior segments of the liver are the most difficult to access and remain one of the limits to laparoscopic liver surgery. Nonetheless, several experienced teams have reported elective resections of these segments with good results [17,57]. Gayet at al. recently reported a series of 62 laparoscopic segmentectomies, 26 of which involved the superior and posterior segments I, IVa, VII and VIII [17]. These resections were associated with increased operative duration (240 vs. 155 min; P < 0.01) and blood loss (350 vs. 100 mL; P = 0.02), compared to the other segmental resections. Segmentectomies VII and VIII were performed through a lateral approach with the patient in left lateral decubitus position, in order to allow correct insertion of intercostal and transdiaphragmatic trocars.

Evolution and perspectives In an effort to make laparoscopy less and less invasive, surgeons have tried to decrease the number of trocars necessary to perform an operation. Single trocar surgery has currently been developed in several domains. Several teams have reported their experience with single incision LLR [58,59]. In highly selected patients, the results of this approach seem comparable to those of traditional laparoscopy. There is probably a slight cosmetic advantage but that is very difficult to evaluate. The resections reported so far have been small, atypical resections or left lobectomies [58,59]. The use of single incision for more complex operations is certainly conceivable, but will probably be performed with robotic assistance. A few cases of Natural Orifice Translumenal Endoscopic Surgery (NOTES) LLR have been reported in the animal model [60] as well as in man [61]. The laparoscopic approach is anecdotal in this indication. The transgastric approach adds the risk associated with intestinal suture for operations that do not require such procedures. Whatever the place of this

approach in the future, robotization may be necessary to make it standard treatment. Because of limited tactile sensation, intra-operative guidance (navigation) during LLR is a future topic of interest. Intra-operative sonography has already been alluded to, but newer ingenious procedures to guide the surgeon are under investigation. Guidance with pre-operative 3-D imaging (augmented reality) is already possible and is used daily in certain specialties such as neurosurgery. In the domain of hepatic surgery, this technique also exists and has a potential role in LLR [62]. But, irrespective of the quality of reconstructions obtained through pre-operative imaging, the surgeon still has to translate the pre-operative images obtained through augmented reality to the actual anatomy in front of his/her eyes. Ideally, the surgeon would be to be able to see the anatomy of the patient in real time. Innovations in this direction have actually been attempted. Chopra et al. [63] reported five case of LLR under intra-operative MRI guidance in a pig model. No ferromagnetic material could be employed in these operations, but aside from some interferences between the camera and the magnetic field, the operations were performed under good conditions. The use of a fluorescent marker to guide LLR for HCC have also been reported [64] as well as the use of indocyanine green coupled with a specific camera to visualize the biliary tree during the operation [65]. Robots are an inevitable part of the future of surgery. Liver laparoscopy will undoubtedly follow along this road. Several teams have reported their preliminary experience with LLR performed with the assistance of the Da Vinci system (Intuitive Surgical, USA) [66—71] (Table 4). Packiam et al. [69] reported 11 cases of left lobectomies performed via robotic laparoscopy. These resections were associated with a higher rate of minor complications as well as higher costs than traditional laparoscopic resections. Troisi et al. [70] reported 40 robotic LLR compared to 223 traditional LLR. In spite of a higher number of minor resections, bleeding (330 vs. 174 mL; P = 0.001) and the conversion rate (20% vs. 7.6%; P = 0.03) were higher in the robotics group. This system clearly allows simplification of certain complex procedures such as major LLR and could facilitate additional procedures such as vascular or biliary reconstruction. Laparoscopic liver resection seems to be a good indication for robotic surgery because it requires a steady operative field. In its present form, however, the use of robots is limited by their costs and the bulk of the apparatus. The present robotic system could, however, be replaced within a few years, by more innovative systems.

Table 4 Intra- and post-operative results after robot-assisted laparoscopic liver resection in series including more than 10 patients. Authors, date

Number Number of of LLR major liver resections

Conversion rate, %

Duration of operation, min

Blood loss, mL

Morbidity, % Length of stay days

Lai et al., 2013 [71] Troisi et al., 2013 [70] Lai et al., 2012 [68] Packiam et al., 2012 [69] Casciola et al., 2011 [67]

42 40 10 11 23

— 20 0 0 8.6

229 271 347 175 280

412 330 407 30 245

7.1 12.5 30 27 13

10 0 10 — 0

6.2 6.1 6.7 4 8.9

LLR: laparoscopic liver resection.



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Laparoscopic liver resection: A review Laparoscopy is also used for living donor partial liver harvesting. Since the first two cases described by Cherqui et al. [72] in 2002, more than 120 living donor LLR have been reported [73]. Such interventions represent a technical challenge and can only be performed in only a few centers with a large experience in hepatic surgery, transplantation and laparoscopy. Soubrane at al. have recently reported the first case of living donor laparoscopic right hepatectomy [74]. Training in LLR requires a long learning curve, before morbidity and conversion rates decline. The number of operations to get beyond the learner’s stage has been evaluated at 60 [75]. As for all evolving surgical techniques, the training of young surgeons in LLR is an immense challenge. Training starts with open hepatic surgery and other simple operations via laparoscopy. Simulators will probably have an important role in the future training of surgeons. One Australian team has developed a simulator for LLR [76] that could eventually allow young surgeons to train in this type of surgery. But training in the operation room should be the first step. It is therefore up to experienced surgeons to launch themselves into this type of surgery, probably the best way to stimulate the younger generation to learn and accomplish these techniques.

Conclusions The High French Authority of Health (Haute Autorité de Santé) evaluated that approximately 200 right hepatectomies had been performed via laparoscopy [77] in France in 2010, i.e. 10 to 20% of all right hepatectomies. In comparison, the number of left colectomies via laparoscopy is about 18,000 (per year, in France) [78]. However, in spite of limited indications, LLR presents enormous advantages. An international prospective randomized study is underway and will perhaps confirm the theoretical advantages of this approach [14]. These advantages should encourage teams specialized in hepatic surgery to learn LLR. Left lobectomy, a relatively simple anatomic resection, is probably best adapted to learn the laparoscopic approach. Atypical resections are sometimes difficult and require more experience. The operative indication must never be modified to suit the experience of the surgeon or the type of approach. The future of laparoscopic hepatic surgery will certainly be influenced by the development of new techniques in intra-operative guidance as well as by robotics.

KEY POINTS • Laparoscopic liver resections (LLR) present considerable advantages: abdominal wall preservation (early return to prior activity, decreased peri-operative pain and cosmetic benefit), diminution of morbidity (reduced blood loss and need for transfusions, less post-operative ascites in the cirrhotic, fewer pulmonary complications), and facilitation of subsequent operations (iterative liver resection, liver transplantation).

7 • The best indications today are solitary liver lesions smaller than 5 cm, located in the anterior segments, distant from the transection lines of anatomic resection, and distant from the hepatic veins and the vena cava. • Left lobectomy is probably the most reproducible of LLR and is presently standardized for several teams. It is the starting point of choice for the training of young surgeons. • Although most solitary tumorectomies or segmentectomies appear to be easily accessible, they are paradoxically more difficult and require much more experience. • Major liver resections, and notably right hepatectomy, should be reserved for expert centers. • LLR for HCC and CRLM are associated with surgical margins equivalent to those of open surgery. Survival is comparable in the majority of the retrospective comparative studies. • The mere ability to perform LLR should not modify the operative indications, especially for benign tumors. The decision to operate should be based on the symptomatic character of the lesion or, for adenoma, the risk of eventual malignant degeneration. • Intra-operative ultrasound guidance should be used. • There is a theoretical risk of gas embolism. Frequent episode of CO2 embolization have been documented during LLR, but without any important clinical repercussion.

Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

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Laparoscopic transthoracic liver resection.

Laparoscopic pancreatic resection-a review.

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Pure Laparoscopic Liver Resection for Malignant Liver Tumor: Anatomic Resection Versus Nonanatomic Resection.

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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.

Laparoscopic liver resection: Toward a truly minimally invasive approach.

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A novel difficulty scoring system for laparoscopic liver resection.

A cadaver lab training facility to facilitate laparoscopic liver resection.

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Comparative study and systematic review of laparoscopic liver resection for hepatocellular carcinoma.