European experience of laparoscopic major hepatectomy

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1 J Hepatobiliary Pancreat Sci (2013) 20: DOI /s TOPICS Laparoscopic major liver resection European experience of laparoscopic major hepatectomy Dimitrios Tzanis Nairuthya Shivathirthan Alexis Laurent Mohammad Abu Hilal Olivier Soubrane Airazat M. Kazaryan Giuseppe Maria Ettore Ronald M. Van Dam Panagiotis Lainas Hadrien Tranchart Bjorn Edwin Giulio Belli Ricardo Robles Campos Neil Pearce Brice Gayet Ibrahim Dagher Published online: 2 October 2012 Ó Japanese Society of Hepato-Biliary-Pancreatic Surgery and Springer 2012 Abstract Background/purpose Laparoscopic hepatectomies have seen a worldwide proliferation. Major anatomic resections, which were initially considered unsuitable for laparoscopy, are currently confined to a few centers of expertise. The aim of this study was to discuss the current trends and techniques in laparoscopic major hepatectomy in Europe. Methods The prospective databases of ten European centers were combined to provide answers to a questionnaire that had been addressed to all European teams known to perform laparoscopic liver surgery. Results Between 1996 and 2011 a total of 2245 laparoscopic liver resections have been carried out, of which 495 (22 %) were major resections. The proportion of laparoscopic right and left hepatectomies varied between 4 and 40 % of all major hepatectomies of the same type. Benign, primary malignant and metastatic lesions were, respectively, 22.4, 19.6 and 58 % of all indications. The different techniques and approaches, as regards hand assistance, hepatic inflow and outflow control, liver mobilization and concomitant colectomies, are discussed. Conclusions To date, an important level of experience of laparoscopic liver resection has been accumulated in Europe, and experience of major hepatectomies is constantly increasing. However, they remain technically very demanding procedures which should be confined to expert surgeons who have already acquired considerable experience with simpler laparoscopic liver resections. D. Tzanis P. Lainas H. Tranchart I. Dagher (&) Department of Digestive and Minimally Invasive Surgery, AP-HP, Antoine Béclère Hospital, 157 rue de la Porte de, Trivaux, Clamart Cedex, France ibrahim.dagher@abc.aphp.fr N. Shivathirthan B. Gayet Department of Digestive Diseases, Montsouris Institute, Paris, France A. Laurent Department of Digestive and Hepatobiliary Surgery and Liver Transplantation, AP-HP, Henri-Mondor Hospital, Créteil, France M. Abu Hilal N. Pearce Hepatobiliary-Pancreatic and Laparoscopic Surgical Unit, Southampton General Hospital, Southampton University Hospitals, NHS Trust, Southampton, UK O. Soubrane Department of Hepatobiliary Surgery and Liver Transplantation, AP-HP, Saint-Antoine Hospital, Paris, France A. M. Kazaryan B. Edwin Department of Hepatopancreatobiliary and Gastrointestinal Surgery, Intervention Centre, Oslo University Hospital-Rikshospitalet, Oslo, Norway G. M. Ettore General Surgery and Transplantation Unit, San Camillo Hospital, Rome, Italy R. M. Van Dam HPB, Minimal Access and Robotic Surgery, Maastricht University Medical Center, Maastricht, The Netherlands G. Belli Department of General and Hepato-Pancreato-Biliary Surgery, S.M. Loreto Nuovo Hospital, Naples, Italy R. R. Campos Department of Hepatobiliary Surgery and Liver Transplantation, University Hospital Virgen de la Arrixaca, El Palmar, Murcia, Spain I. Dagher Paris-Sud University, Orsay, France

2 J Hepatobiliary Pancreat Sci (2013) 20: Keywords Laparoscopy Major hepatectomy Right hepatectomy Left hepatectomy Introduction Almost 20 years after the first laparoscopic liver resection [1], laparoscopic hepatic surgery has seen a worldwide expansion [2 4]. European experience, which started in the mid-1990s with the first cohort of patients published in 2000 [5], has made important steps forward and even demonstrated the benefits of laparoscopy in major resections [6]. Major hepatectomies performed using the laparoscopic approach had already been reported since 1998 [7]. However, there has been a much slower proliferation, internationally and in Europe, as compared with other minimally invasive procedures. This can be attributed to the complexity of the procedures and fear of uncontrolled hemorrhage, combined with high-level technical demands and lack of training opportunities for most surgeons. However, progress in technology and better understanding of hepatic and minimally invasive surgery have resulted in some reports of medium-sized series of major laparoscopic hepatectomies with encouraging results [6, 8, 9]. Much better supported by multi-center international studies [10], major hepatic procedures using minimally invasive approaches still remain confined to a few centers worldwide, with experienced surgeons, already familiar with simpler laparoscopic hepatic resections [11]. Ten European centers which are actively involved in the development of laparoscopic liver surgery participated in the current study: 4 centers from France, 1 from UK, 2 from Italy, 1 from Norway, 1 from Spain and 1 from the Netherlands. The aim of this multicenter study is mainly to discuss current trends in the application of minimally invasive techniques to major hepatic resections in Europe, in spite of differences in technical issues and approaches which are under continuous evolution. Patients and methods All 10 specialized units already had significant experience of open hepatic surgery before moving on to laparoscopic procedures and kept a prospective database of all liver resections. Experience in minimally invasive procedures for liver surgery was initiated with minor resections and left lateral sectionectomies. Major hepatic resections were attempted after having acquired considerable experience with less-demanding operations. The laparoscopic approach was first employed in the mid-1990s, in the French units, while other units followed shortly afterwards. Consent was obtained from all patients, who were informed of the innovative character of the procedures. To date, 15-years experience of laparoscopic hepatic surgery has already accumulated in Europe. Adapted questionnaires were sent to all European centers known to practice laparoscopic liver surgery in order to gather the most recent data. Elements demanded by the questionnaires included total number of laparoscopic hepatic resections, number of laparoscopic major hepatectomies, indications, number of procedures performed for cirrhotic patients, details on technical points, blood loss and duration of interventions. The technical points that were especially discussed were the use of hand assistance, the application of vascular control of inflow and outflow before parenchymal transection and simultaneous procedures. Ten centers responded to our request. A final table pooling the information from all questionnaires was created and used for final interpretation of data and analysis. All centers share similar criteria to select patients eligible for laparoscopy in major liver resections: tumor criteria include size of lesions (B5 cm), safe distance from major vessels and transection lines, and noneed for vascular or biliary reconstruction. Liver criteria include non-cirrhotic or compensated cirrhotic livers with esophageal varices Bstage 1 and a platelet count C /L. The ASA score should be B3. Results From 1996 to the end of 2011, a total of 2245 laparoscopic liver resections were carried out in these European centers, of which 495 (22 %) were major hepatectomies: these include 348 laparoscopic right hepatectomies (LRH), 108 laparoscopic left hepatectomies (LLH), 5 central hepatectomies and 34 trisegmentectomies (Table 1). Indications were: benign lesions (22.4 %), primary malignant tumors (19.6 %) and metastatic lesions (58 %). In the different centers, the percentage of LRH and LLH varied between 4 and 40 % of all major hepatectomies of the same type. Thirty-seven of 348 (10.6 %) LRH and 13 of 108 (12 %) LLH were performed in cirrhotic patients. Only two European centers use hand assistance routinely. In the other centers, it was used only selectively, mostly near the beginning of the experience in some cases of LRH in three of the centers. With regard to vascular inflow control, portal triad clamping is used routinely by only 2 teams. Portal veins and hepatic arteries are controlled extraparenchymally sporadically by 9 teams before parenchymal transection with very few exceptions. Division of the bile duct is performed intraparenchymally by 3 teams.

3 122 J Hepatobiliary Pancreat Sci (2013) 20: Table 1 Types of resection and indications for major laparoscopic liver resections Laparoscopic liver resections, n 2245 Laparoscopic major liver resections, n (%) 495 (22) Right hepatectomy, n (%) 348 (70.3) Left hepatectomy, n (%) 108 (21.8) Central hepatectomy, n (%) 5 (1) Trisegmentectomy, n (%) 34 (6.9) Concomitant colon resections a, n (%) 8 (1.6) Cirrhotic patients, n (%) 50 (10.1) Indications Benign lesions, n (%) 111 (22.4) Primary malignant tumors, n (%) 97 (19.6) Metastases, n (%) 287 (58) a 3 centers The different centers do not share the same opinion on mobilization of the liver and hepatic vein control prior to parenchymal transection. Five centers always mobilize the liver, 1 center does so only for LLH but never for LRH, and two centers perform LRH both ways. Among those who perform liver mobilization, 2 teams routinely control the hepatic veins before moving on to transection. Concomitant colon resections were performed in three centers: 6 colonic resections were performed at the same time as LRH and another 2 during LLH. For 9 centers for which data are available, the rate of conversion for both LRH and LLH was 10.8 % (49/451). Mean operating times (data available for 9 centers) were 301 min for LRH and 250 min for LLH. Mean blood loss for the same centers was 437 and 275 ml for LRH and LLH, respectively (Table 2). Discussion Laparoscopic liver resections have seen a very important expansion all over the world in the last 15 years [2 4], which has created a need for an international consensus on laparoscopic hepatic surgery [11]. This sudden proliferation concerns mainly minor hepatectomies (resection of less than 3 segments), and, until recently, only sporadic reports of major laparoscopic liver resections existed [3, 4, 6, 9, 12 14]. In 2009, a multicenter international study by Dagher et al. [10] of 210 major liver resections using laparoscopy, demonstrated that laparoscopic major hepatectomies are feasible in selected patients, when performed by experienced surgeons. It has also been demonstrated that, when laparoscopy is employed for major resections, there is a benefit in terms of blood loss, general morbidity and length of hospital stay [6]. However, it is evident that major resections represent a rather small percentage of all Table 2 Intraoperative results Mean duration of surgery right hepatectomy, min 301 Mean duration of surgery left hepatectomy, min 250 Estimated blood loss right hepatectomy, ml 437 Estimated blood loss left hepatectomy, ml 275 Conversions, n (%) 49 (10.8) Data for 9 centers laparoscopic hepatectomies, remain challenging and demand both laparoscopic and hepatic surgery expertise. And, when all this is guaranteed, considerable experience of simpler laparoscopic hepatic procedures is prerequisite before attempting major resections. Patient selection is a major issue that should be well defined. In our study, all participating teams shared very similar selection criteria. Tumors should be located at a safe distance from the potential transection line on preoperative imaging and not close to major vascular structures. Although a considerable distance from hepatic veins is clearly needed, we believe that tumor proximity to the liver hilum could be favorably handled by laparoscopy because of the magnification and high quality of the image. Tumor size is another consideration: it has generally been accepted and reported that tumors should be smaller than 5 cm. It is our opinion that tumor size on its own is no longer a contraindication, but tumor localization should also be evaluated; posterior tumors or tumors with extrahepatic development can be much bigger without causing significant difficulty. Colonic resections have very rarely been combined with major laparoscopic procedures. In this study only 6 colectomies were performed concomitantly with LRH and another 2 with LLH. Despite technical difficulties which render simultaneous resections even more demanding, we believe that the important advantages of laparoscopy make it a reliable alternative for concomitant procedures. With regard to indications for surgery, it remains our strong belief that the laparoscopic approach should not broaden the indications for resection of benign tumors. Benign tumors represent a good indication when the diagnosis is uncertain, when they are symptomatic, when malignant degeneration is possible, and when there is a significant risk of hemorrhage. On the other hand, benign tumors in this study constitute an important proportion of all indications for major hepatectomy: this underlines the fact that, because of all the advantages of minimal invasiveness, the laparoscopic approach is preferred for this type of lesion. We consider that the percentage of compensated cirrhotic patients in this European series is important (10.6 % for LRH and 12 % for LLH). We feel that this probably

4 J Hepatobiliary Pancreat Sci (2013) 20: demonstrates that surgeons are becoming convinced of the advantages of laparoscopy in cirrhosis. The proportion of major hepatectomies performed by laparoscopy as a percentage of all major resections varies considerably between the different centers, between 4 % and 40 %. This is usually correlated with the degree of experience. Centers with large numbers of patients more frequently choose the laparoscopic approach to perform their major resections. Hand assistance has never been very popular among European surgeons. It was seldom used, mostly during early experience, selectively for posterior tumors or when a concomitant colonic resection was planned. Some of the participating centers have never used hand assistance. It has been reported that tactile sensation, easier mobilization of the heavy organ, potentially safer hemorrhage control and more accurate tumor staging represent the most important benefits of hand-assisted techniques [15]. To our knowledge, the only available data on comparison between handassisted and pure laparoscopy is in the study by Dagher et al. [10]. Their conclusions were favorable for hand assistance regarding operative time and hospital stay, but, as stated by the authors, these differences should be prudently evaluated because they could represent a health system bias: hand assistance is much more frequently employed in the United States. European experience, as it has rarely used hand assistance, has little to add to this debate. The issue of vascular inflow control is not treated in the same manner by all teams: only 2 centers routinely perform portal triad clamping. Portal pedicles are mostly dissected and divided extraparenchymally; 3 teams divide the bile duct intraparenchymally. On the other hand, the strategy for early liver mobilization and control (with or without division) of hepatic veins prior to liver parenchyma transection is not unanimous. Almost all possible combinations can be found among the 10 European centers. The commonest source of bleeding is parenchymal transection. Many different techniques of dividing liver parenchyma have been employed according to surgeons preferences. In this study, mean blood loss was 437 and 275 ml for LRH and LLH, respectively. Although some data are missing, the differences between the participating centers could not be directly correlated with the devices used for transection. In any case, bleeding is always an important issue in laparoscopic hepatectomies; it is probably the parameter that most frequently causes fear among surgeons. Thus, surgeons who perform laparoscopic hepatic resections should be familiar with laparoscopic suturing. Hemorrhage control can be temporarily obtained by using simple techniques, such as compression of the source of bleeding, sometimes by the liver itself, in order to achieve control under stabilized conditions. Conversion, in such cases, should be considered a prudent act, rather than a technical failure. In this study, conversion rates were found to be 10.8 % for LRH and LLH, which is close to rates previously reported [10]. Mean operative times (301 min for LRH and 250 min for LLH) were similar among the centers for which precise data were available and are also similar to those previously published [10]. It is evident, that, despite the worldwide expansion of laparoscopic hepatic surgery, and despite the fact that laparoscopic left lateral sectionectomy is considered the procedure of choice [10], major hepatic resections still remain challenging and confined to very experienced surgeons. Credentialing remains the final challenging issue, as lack of consistent training is often the reality. We believe that surgeons who would like to embark on laparoscopic liver surgery should be familiar with both open hepatic surgery and minimally invasive procedures. Also, before attempting major resections, the surgeon should have accumulated considerable experience with left lateral sectionectomies and minor non-anatomic resections. Laparoscopic major hepatectomies should be in the hands of such experts in order to be feasible and safe. References 1. Gagner M, Rheault M, Dubuc J. Laparoscopic partial hepatectomy for liver tumor. Surg Endosc. 1992;6: Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection 2804 patients. Ann Surg. 2009;250: Buell JF, Thomas MT, Rudich S, Marvin M, Nagubandi R, Ravindra KV, et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248: Koffron AJ, Auffenberg G, Kung R, Abecassis M. Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg. 2007;246: Cherqui D, Husson E, Hammoud R, Malassagne B, Stéphan F, Bensaid S, et al. Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg. 2000;232: Dagher I, Di Giuro G, Dubrez J, Lainas P, Smadja C, Franco D. Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg. 2009;198: Huscher CG, Lirici MM, Chiodini S. Laparoscopic liver resections. Semin Laparosc Surg. 1998;5: Vibert E, Kouider A, Gayet B. Laparoscopic anatomic liver resection. HPB. 2004;6: Pearce NW, Di Fabio F, Teng MJ, Syed S, Primrose JN, Abu Hilal M. Laparoscopic right hepatectomy: a challenging but feasible, safe and efficient procedure. Am J Surg. 2011;202:e Dagher I, O Rourke N, Geller DA, Cherqui D, Belli G, Gamblin TC, et al. Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg. 2009;250: Buell JF, Cherqui D, Geller DA, O Rourke N, Iannitti D, Dagher I, et al. The international position on laparoscopic liver surgery. The Louisville statement, Ann Surg. 2009;250: Dagher I, Caillard C, Proske JM, Carloni A, Lainas P, Franco D. Laparoscopic right hepatectomy: original technique and results. J Am Coll Surg. 2008;206: O Rourke N, Fielding G. Laparoscopic right hepatectomy: surgical technique. J Gastrointest Surg. 2004;8:213 6.

5 124 J Hepatobiliary Pancreat Sci (2013) 20: Gayet B, Cavaliere D, Vibert E, Perniceni T, Levard H, Denet C, et al. Totally laparoscopic right hepatectomy. Am J Surg. 2007; 194: Huang MT, Wei PL, Wang W, Li CJ, Lee YC, Wu CH, et al. A series of laparoscopic liver resections with or without HALS in patients with hepatic tumors. J Gastrointest Surg. 2009;13:

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