Systematic Reviews
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Oct 7, 2014; 20(37): 13599-13606
Published online Oct 7, 2014. doi: 10.3748/wjg.v20.i37.13599
Laparoscopic liver resection for malignancy: A review of the literature
Eyas Alkhalili, Eren Berber
Eyas Alkhalili, Eren Berber, Department of General Surgery, Cleveland Clinic, Cleveland, OH 44195, United States
Author contributions: All authors contributed to this work.
Correspondence to: Eren Berber, MD, Assistant Professor of Surgery, Department of General Surgery, Cleveland Clinic, 9500 Euclid Avenue/F20, Cleveland, OH 44195, United States. berbere@ccf.org
Telephone: +1-121-64450555 Fax: +1-121-66360662
Received: November 27, 2013
Revised: May 13, 2014
Accepted: June 2, 2014
Published online: October 7, 2014

Abstract

AIM: To review the published literature about laparoscopic liver resection for malignancy.

METHODS: A PubMed search was performed for original published studies until June 2013 and original series containing at least 30 patients were reviewed.

RESULTS: All forms of hepatic resections have been described ranging from simple wedge resections to extended right or left hepatectomies. The usual approach is pure laparoscopic, but hand-assisted, as well as robotic approaches have been described. Most studies showed comparable results to open resection in terms of operative blood loss, postoperative morbidity and mortality. Many of them showed decreased postoperative pain, shorter hospital stays, and even lower costs. Oncological results including resection margin status and long-term survival were not inferior to open resection.

CONCLUSION: In the hands of experienced surgeons, laparoscopic liver resection for malignant lesions is safe and offers some short-term advantages over open resection. Oncologically, similar survival rates have been observed in patients treated with the laparoscopic approach when compared to their open resection counterparts.

Key Words: Laparoscopic liver resection, Laparoscopy, Laparoscopic liver surgery, Hepatectomy, Liver malignancy

Core tip: This paper is a review article of laparoscopic liver resection for malignancy. We review all large studies that investigated the techniques and outcomes of laparoscopic liver resection as well as those comparing laparoscopic to open resections.


Citation: Alkhalili E, Berber E. Laparoscopic liver resection for malignancy: A review of the literature. World J Gastroenterol 2014; 20(37): 13599-13606
INTRODUCTION

Twenty-years after the first reported laparoscopic liver resection by Gagner et al[1], there has been an exponential growth of reports of laparoscopic liver resections but the results are yet to be fully elucidated.

Although initially described for benign and peripheral lesions, 50% of overall laparoscopic liver resections are now performed for malignant lesions[2] and a growing number of centers are now performing major resections, including right and left hepatectomies, in North America, Europe, and Asia[3-8].

The purpose of this study is to review the published literature on laparoscopic liver resection for malignant lesions. We will discuss the different types of resection, the most common as well as the innovative techniques, the surgical outcomes, postoperative complications, and oncologic results.

MATERIALS AND METHODS

A PubMed search was performed for original published studies until June 2013. Articles were selected using the indexing terms “hepatectomy”, “laparoscopy”, and “liver neoplasm/surgery”. Keyword search for “laparoscopy”, “laparoscopic”, “hepatectomy”, “resection”, “liver cancer”, “liver neoplasm”, “liver tumor”, “hepatic cancer”, and “hepatic neoplasm”. Large series with more than 30 patients with malignant lesions were included. Reported procedure other than resection, such as radiofrequency ablation and cyst fenestration were excluded.

RESULTS

About 43 studies with more than 30 patients who underwent laparoscopic resection for liver malignancy were identified. No randomized clinical trials were available. Most data were reported as case series or case-control studies. Although the first large series was in 2002, the vast majority of reports were published in and after 2009. In this review, we analyzed preoperative findings such as indications and tumor size, intraoperative findings like blood loss and operative time, short-term outcomes, as well as oncologic outcomes (Table 1).

Table 1 Published studies of laparoscopic liver resection for malignancy.
Ref.YearnHCCCRMGB CACholangioLypmhomaNET metsOtherSize (cm)EBL (mL)ConversionOT (min)MDeathLOS (d)Margin (cm)
Choi et al[23]20135757000000.8-5.5150-800NA95-380NA05 172.08 ± 1.68
Guerron et al[63]201340403.3376 ± 1225%239 ± 1715%NA3.71 ± 0.2
Gumbs et al[21]2012404306145NA3006%26511.30%NA6 (1-31)NA
Abu Hilal et al[13]201213318832217110.5-14(10-4000)NA30-5400 40 %NA0 15Pos 0-35%
Topal et al[24]201281NA50 (10-300)NA120 (80-200)11%05 (3-7)NA
Yoon et al[25]201289893 ± 1.6NA4.70%2675 ± 138NANANA1.4 ± 1.4
Cannon et al[26]20123535NA202NANA23%04.8 vs 8.3Neg 97%
Ikeda et al[27]201230161312.6 ± 1146 (0-550)079-697NA05-445 (1-30)
Dagher et al[28]20101631633.6 (1-20)250 (30-2000)9.20%180 (60-655)11.60%1.20%7 (2-76)12 (0-58)
Shafaee et al[29]2011663551320.5-12.5300 (0-5000)11%180 (80-570)26%06 (2-42)0.3 (0-4)
Lai et al[30]20115642140.9-5.4175 (5-2000)3.60%150 (75-307)14.30%06.5 (2-13)89.3% R0
Belli et al[31]201165653.8 (1-9)311 ± 18010.70%NA20%1.50%8.2 (3-15)NA
Truant et al[32]201136362.9 ± 1.2452 ± 44219.40%NA250NA0.95
Nguyen et al[43]20111083.2101NA256NANANA1.12, 1.5
Lee et al[33]201131312.5 (1.5-9)150 (10-1610)18.20%225 (100-420)6.10%05 (2-15)1.8 (0-4)
Hu et al[34]201130306.7 ± 3.1520 ± 30NA180 ± 4513.30%NA13 ± 2.1NA
Kazaryan et al[35]20101071073 (0.5-12)300 (50-4000)4.20%188 (64-488)NA0.90%3 (1-42)NA
Martin et al[5]20106514%48%12%26%4 (2-15)150 (20-1000)4%140 (50-240)23%1%3 (1-13)Pos 3%
Zhang et al[41]20107029282110NA8.80%150 (20-390)14.80%06 (1-20)Neg 100%
Tranchart et al[36]201042423.58 ± 1.75346 ± 435.7NA233.1 ± 92.720.40%2.40%6.7 ± 5.91.04 ± 0.8
Yoon et al[8]201069693.1 ± 1.57.20%280.9 ± 128.221.70%NA9.9 ± 5.61.5 ± 1.6
Nguyen et al[62]2009109109NA200 (20-2500)3.70%234 (60-555)12.00%NA4 (1-22)Neg 94.4%
Sasaki et al[37]20097237352.5 (1.5-8.5)64 (1-917)NA177 (70-430)5.50%NA8.5-100.6 (0-4)
Bryant et al[16]20091006422311NA(0-2000)9.60%30-48015.10%07.9 (2-76)1.53 (0-5.8)
Inagaki et al[38]2009523610333.1 ± 1.8393 ± 5642.90%214 ± 9310%NA17NA
Cho et al[4]2009352783.4 (1.5-7.5)619.5 (20-1800)NA299.9 (80-630)27.50%NA10.9 (5-38)1.3 (0.2-5)
Huang et al[39]200933273123.4 (1-11)200 (100-400)6.70%120 (90-177.5)11.11%NA50.2-3.2
Otsuka et al[40]2009765516233.68 ± 2.8262 ± 344.8NA268 ± 123.111%011.8 ± 7.3NA
Castaing et al[14]200960603.3 ± 1.1NA10%NA27%1.70%10 (5-50)Neg 87%
Dagher et al[3]2009210NA300 ± 39112%250 ± 103.822%1.00%6 ± 3.510.5 ± 13.6
Zhang et al[41]2009493310636.2 (0.8-15)280 (10-1000)NANANA0NA1.2 (0.5-6)
Cho et al[42]20087152193.7 ± 3425 (20-900)5%240 (30-540)15%09 (4-21)1 (0.3-6.8)
Topal et al[6]2008773.8 (0.5-17)500 (10-7000)9%95 (30-385)5.50%NA6 (0-41)Pos in 1.2%
Chen et al[53]20081161161.3-5.1101.6-667.2NA118.4-488.76%NA6NA
Buell et al[17]200810636318313.1-6.4NANANA3.70%NA2.80%
Hompes et al[22]20074583214114 (0.8-17)200 (5-4000)6.60%115 (45-360)24%07 (3-41)1 (0.1-3)
Dagher et al[47]200738249323.8 (2.2-8)397 (100-2300)10%227 ± 10916%1.40%5.9 ± 5.61.1 (0.1-3.2)
Koffron et al[48]2007103NA1026% to ha999.30%0NANA
Vibert et al[9]20066516412330.8-18NA13%85-51519%1.10%11 (3-47)NA
Mala et al[10]200547142133 (0.8-15)700 (< 100-5000)6%187 (80-334)16%03.5 (1-14)Pos in 6%
O'Rourke et al[7]2004332211NA20-20009.40%40-37014%0NA1.1 (0-3)
Inagaki et al[45]200352363.1 (1-14)393 ± 564 (5-3500)2.90%214 (61-375)26.40%014.8NA
Gigot et al[59]20023710125103.3 (1-6)NA10.80%NA21%07 (2-16)Pos in 6.7%
DISCUSSION
Indications and contraindications of laparoscopic liver resection

As with open surgery, hepatocellular carcinoma (HCC) and colorectal metastasis (CRM) are the main indications of malignant tumor resection[2,3,6,9-15]. Much less commonly, resections of cholangiocarcinoma, lymphoma, and non-colorectal liver metastasis (e.g., neuroendocrine tumors, breast cancer, and renal cell carcinoma) have been performed[9,13,15-18].

In patients who cannot tolerate pneumoperitonium due to their cardiopulmonary status and those with adhesions that cannot be lysed laparoscopically, laparoscopic liver resection is contraindicated. Relative contraindications are in patients with lesions adjacent to the inferior vena cava or major vessels, in whom there is a need for biliary and/or vascular reconstruction, those with hilar lesions or in those with resections that require an extensive portal lymphadenectomy[2,19,20]. Although considered a contraindication for laparoscopic resection by a large number of surgeons, successful minimally invasive approach to gallbladder cancer has been performed in 7 patients published in two papers with no reports of port site metastasis[21,22].

Minor resection

Minor resections including segmentectomy, subsegmentectomy, and wedge resections are the most common type of laparoscopic liver resection performed. Left lateral sectionectomy (LLS) which was first reported by Azagra et al[44], is by far the most frequently reported anatomic resection given easy visualization of the lesions with laparoscopy, peripheral location of the intended resection area, and the ease of controlling the left hepatic vein. Inagaki et al[45] reported 30 LLS for hepatocellular carcinoma using Hand-assisted technique. They postulated 2 advantages to the Hand-assisted technique; First, better visualization of the surgical field and the transected margin with direct manipulation by the surgeon’s hand, and second, immediate hemostasis by depressing the bleeding point and proper application of hemostatic instruments.

Major resection

After the first reported cases of laparoscopic major hepatectomy by Hüscher et al[46] in 1998, an increasing number of series describing major resections have been reported[6,13,14,17,23,25-27,47,48].

In the largest series of major hepatectomies of 210 patients, 136 with right hepatectomoies and 74 with left hepatectomies, Dagher et al[3] showed a mean operative time of 250 min, with mean EBL of 300 mL. The mortality in that series was 1%.

Gumbs et al[49,50] reported the first laparoscopic extended left hepatectomy as well as the first laparoscopic extended right hepatectomy in 2008. The patient who underwent laparoscopic extended right hepatectomy had gallbladder adenocarcinoma and underwent preoperative portal vein embolization followed by totally laparoscopic extended right hepatic resection with preservation of segment IVa and the left half of IVb due to concerns of postoperative hepatic reserve. A total of 3 patients underwent laparoscopic extended left hepatectomy. One patient suffered a bile leak that was treated with endoscopic biliary stents.

Three large series have also included patients who underwent extended hepatectomy[14,26,29]. The papers showed that extended hepatectomy can be safely performed when undertaken by experienced surgeons and with careful patient selection.

Uncommon resections and novel approaches

While laparoscopic resection of lesions in segments 2-6, the so called “laparoscopic liver segments” have been widely performed, posterior and superior lesions have been classically unamenable to laparoscopic resection. This has changed in the last 6 years.

In a series of 300 patients, including 103 with malignant liver tumors, Koffron et al[48] reported 8 caudate lobectomies, 2 of which were for cancer. Cho et al[42] documented 10 right posterior segmentectomies in a series of 71 patients with hepatocellular carcinoma and colorectal metastasis.

Abu Hilal et al[51] reported 2 cases of pure laparoscopic en bloc left hemihepatectomy and caudate lobe resection for intrahepatic cholangiocarcinoma. The first patient’s operative time was 360 min and blood loss was 390 mL. The second patient’s operative time was 310 min and blood loss was 300 mL.

Hu et al[52] reported a case of multiple hepatic colorectal metastases of the left lateral and right posterior segments who underwent laparoscopic partial hepatectomy of the right posterior segment using a retroperitoneal approach, followed by laparoscopic hepatic left-lateral segmentectomy using a transabdominal approach. The operative time was 120 min, blood loss volume was 150 mL and the patient was discharged on postoperative day 9.

Hand-assisted technique

Hand-assisted technique entails the creation of a 7-8 cm incision that would allow the operating surgeons’ hand access to the abdominal cavity through a gas-tight port. The theoretical advantages of the hand-assisted technique is the ability to apply liver traction and mobilization, palpate the liver with tactile feedback, and help achieve hemostasis by applying compression[17,45,48].

The Hand-assisted technique has been proposed to provide a safer and more attainable approach to laparoscopic resection[17,48]. The application of the hand-assisted technique has been proposed to help with difficult resections like those involving the posterior-superior segments[53]. In their published series in 2007, Koffron et al[48] reported 103 patients with laparoscopic liver resection. In 6% of the patients a conversion from a totally laparoscopic to hand-assisted surgery was necessary while the conversion to open surgery was nil. They suggested that the use of hand-assistance may help prevent conversion to open surgery. However, there is no consensus on the usefulness of the hand-assisted technique as other authors have doubted its usefulness[7,54].

Robotic resection

Robotic laparoscopic resections are now well reported in the literature. While the technique of port placement is different from laparoscopic surgery, most studies have showed encouraging results with comparable results to laparoscopic approach[55]. In a series of 70 patients, 42 of which had malignant lesions, Giulianotti et al[56] reported 4 conversions to open surgery (5.7%), a median operative time for a major resection of 313 min and 198 min for minor resection, median blood loss of 150 mL for minor resection and 300 mL for major resection. The rate of complications was 21%, while the mortality rate was 0%.

In a matched analysis study, Daouadi et al[57] showed that patients undergoing robotic liver resection had longer operative times when compared to laparoscopic resection (253 min vs 199 min), however, the robotic approach increased the percentage of major hepatectomies that were completed in a purely minimally invasive approach. There was no difference between the two groups in term of other surgical outcomes like blood loss, resection margin, and 3-mo mortality.

Operative technical details

Precoagulation of the surface of hepatic parenchyma using a variety of instruments and techniques like the Salient monopolar Endo FB 3.0 or Endo SH 2.0 (Salient Surgical Technologies, Inc., Dover, NH, United States) combined with the Microtaze (Alfresa-Pharma Co., Inc., Osaka, Japan), the Cool-tipTM RFA system (Valleylab, Tyco Healthcare, Mansfield, Massachusetts, United States), and Radiofrequency precoagulation (Laparoscopic Habib 4 ×, Angiodynamics, Queensbury) was postulated as a way to help reduce blood loss by many authors[37,40,53].

The most commonly used equipment for parenchymal transection were the Harmonic scalpel (Ethicon Endo-Surgery), the laparoscopic ultrasonic surgical system (USU; Olympus Optical, Tokyo, Japan), and Cavitron Ultrasonic Surgical Aspirator CUSA (Valleylab)[13,30,32,37,38,58].

Other less common techniques included the use of staplers[17,30,38] and crush-clamp technique[40]. These are largely dependent on surgeon or center preference.

The Pringle maneuver in which the portal triad is clamped is the most common method used to minimize blood loss during liver resections. There was no consensus in the published literature as to the role of the Pringle maneuver in laparoscopic resections. It was used intermittently by some groups to reduce blood loss[13,30,32].

Belli et al[31] described the laparoscopic application of Pringle maneuver using tape that was placed around the porta hepatis by the use of Endo Retract TM Maxi (Tyco Healthcare, Norwalk, Conn., United States). This was passed through a 16-Fr rubber drain and used as a tourniquet when necessary[31]. Others, like Tranchart et al[58], purposely didn’t use the Pringle maneuver although an explanation to this approach was not provided.

A number of studies have reported that inflow occlusion is required less often and for shorter periods during laparoscopic liver resections[5,35,48]. This was postulated to be due to the magnification and improved visualization of the hepatic parenchyma as well as the tamponade effect of pneumoperitonium on venous bleeding.

Outcomes of laparoscopic liver resection

Operative blood loss: Due to the heterogeneity of the reported cases, blood loss was highly variable in different studies. Average blood loss ranged between 50 to 700 mL. Dagher et al[28] and Otsuka et al[40] showed that with late experience, blood loss was significantly lower than in early cases, i.e., surgeons had lower blood loss during laparoscopic resection with more procedure performed. Six studies have showed that laparoscopic resection was associated with lower blood loss than open surgery[5,6,24,26,48,58]. Martin et al[5] showed lower rates of transfusions in laparoscopic resections when compared to open resections (10% vs 48%).

Operative time: In terms of Operative time, the average operative time ranged from 95 to 280 min. Although one study showed increased operative time when compared to open surgery[33], 3 studies demonstrated decreased operative time in laparoscopic surgery[5,24,48]. Dagher et al[47] showed decreased operative times when early experience is compared to an established technique period. (270 ± 143 min vs 171 ± 95 min, P < 0.001), which points out that there is a learning curve with laparoscopic liver surgery.

Conversion to open surgery and length of stay: Conversion to laparotomy rates in the literature ranged from 0% to 19.4%. Koffron et al[48] converted to Hand-assisted technique in 6% of the resections and had 0% conversion to open surgery which signifies that the use of the hand-assisted technique may decrease the rate of conversion to open surgery. Ikeda et al[27] had a 0% conversion rate in a series of 30 patients. In the series published after 2011, conversion rates never exceeded 6%, which also may point to a learning curve effect in laparoscopic liver surgery. The main reasons for conversion were bleeding, adhesions, and inability to complete the resection laparoscopically due to technical or anatomical considerations.

The average length of stay ranged from 4.8 to 13 d in the studies and many of them found a shorter length of stay when compared to open surgery[4-6,26,33,53,58].

Morbidity and mortality: The average morbidity rate was 5.5% to 27.5%. Common complications included bile leak, liver abscess, and transient hepatic failure. General complications included pleural effusions, pneumonia, urinary tract infection, and cardiac arrhythmia. Lower morbidity as compared to open surgery was observed in many studies[5,6,24,26,48].

Inagaki et al[38] showed markedly decreased rate of pulmonary complications in the patients who underwent laparoscopic resection as compared to open surgery (3% vs 17%).

Mortality rate varied between 0% and 3.7%. Reported causes of death included liver failure[28,58], cerebral infarction secondary to hypotension[9], postoperative hepatorenal failure[17], pseudomembranous colitis, technical clip failure leading to massive hemorrhage[14], acute respiratory distress syndrome[28,31], bleeding from esophageal varices[13], and multi-organ failure[35].

Potential disadvantages: While the safety of laparoscopic liver resection has been documented, possible limitations include the significant learning curve[47], loss of tactile feedback and inability to manually palpate the liver that may cause missing other lesions, and potential bleeding that may be harder to control laparoscopically[2].

Oncologic results

Resection margin: The surgical margins were free of cancer in 87% to 100% of patients in the published studies. The Size of the margin varied with an average ranging between 0.3 cm to 2.08 cm. Topal et al[6] showed a lower rate of positive surgical margin with laparoscopic surgery as opposed to open resection; 1.2% vs 2.1%.

Castaing also showed higher rate of R0 resection with laparoscopic resection 87% compared to open surgery 72%[14]. The addition of intraoperative ultrasound was associated with lower rate of positive margins[59]. Buell et al[17] reported the only case of port site metastasis in the literature which was in a patient who underwent laparoscopic resection for CRM.

Hepatocellular carcinoma: Hepatocellular carcinoma is the most common primary liver malignancy. 52% of reported laparoscopic liver resections done for malignancy are performed for HCC[2]. In the literature, the 3-year disease-free survival was 51% to 62% and the overall 3-year survival ranged from 66.4% to 90.4%. The 5-year disease-free survival ranged from 32% to 46.4%, while 5-year overall survival was 50% to 85.9% (Table 2).

Table 2 Reported survival after laparoscopic resection for hepatocellular carcinoma.
Ref.Disease-free survival
Overall survival
1 yr2 yr3 yr5 yr1 yr2 yr3 yr5 yr
Gigot et al[59]43.70%62.50%
Chen et al[53]85.4%-94.7%66.4%-74.2%59.4%-61.7%
Tranchart et al[36]60.90%45.60%74.40%59.50%
Yoon et al[8]60.40%90.40%
Lai et al[30]85%47%38%96%67%52%
Belli et al[31]81%62%32%95%70%55%
Truant et al[32]35.50%70%
Lee et al[33]78.80%51%45.30%86.90%81.80%76%
Hu et al[34]50%
Yoon et al[25]52.90%46.40%93.30%85.90%
Choi et al[23]71%81%
Inagaki et al[45]79.30%

Three studies found no difference in survival between patients with hepatocellular carcinoma who were treated with laparoscopic resection when compared to open resection[32,33,52].

Belli et al[60] showed reduced morbidity, especially postoperative ascites, and a shorter length of stay in cirrhotic patients who underwent laparoscopic resection for hepatocellular carcinoma when compared to those who underwent open resection.

In the largest series of 163 patients with hepatocellular carcinoma treated at 3 European centers by Dagher et al[28], the mean operative time was 180 min, mean estimated blood loss was 250 mL, the mortality rate was 1.2% and the mean resection margin was 1.2 cm. The researchers also found that there has been a decrease in operative time and blood loss, increase in the size of tumors resected, and lower rate of morbidity in patients who were operated on in the later experience series[28].

Colorectal liver metastasis

Surgery is the only curative option for metastatic colorectal cancer to the liver. 35% of laparoscopic liver resections for malignancy are performed for CRM[2].

The goal of resection in patients with CRM is resection of all liver metastasis with a negative margin but at the same time preserving adequate post-resection liver volume. Liver resection offers long-term survival in up to 60% of patients with CRM[61].

Disease-free survival at 1 year was 61.3% to 81%, but dropped at 5 years to 30% to 42%. Overall survival at 1 year was 88% to 100%, at 3 years ranged from 82% to 88%, and at 5 years ranged from 51% to 64% (Table 3).

Table 3 Reported survival after laparoscopic resection for colorectal metastasis.
Ref.Disease-free survival
Overall survival
1 yr2 yr3 yr5 yr1 yr2 yr3 yr5 yr
Gigot et al[59]53.3%100%
O’Rourke et al[7]81%88%
Castaing et al[14]65%30%30%97%82%64%
Shafaee et al[29]27%83%55%
Lai et al[30]92%72%100%88%
Topal et al[24]61.3%41.8%29.9%94.5%83.5%59.5%
Nguyen et al[62]65%43%43%88%69%50%

Nguyen et al[62] reported the largest series of 109 patients with laparoscopic resection for CRM. The mean estimated blood loss was 200 mL, the transfusion rate was 10%, the average length of operation was 234 min, the resection margin was negative in 94.4%, and the conversion rate was 3.7%. Conversion was due to hemorrhage.

Shafaee et al[29] showed that the survival rates for patients undergoing repeat hepatectomy laparoscopically were equivalent or even superior to the long-term outcomes of patients undergoing open resection. Two other studies have showed no statistical difference in disease-free and overall survival rates between laparoscopic and open surgery[14,24].

CONCLUSION

In conclusion, Although laparoscopic liver surgery requires a great deal of experience by hepatobiliary surgeons, this approach is deemed safe for malignant liver lesions with comparable oncological results to open surgery. In addition, it offers better short term results including shorter hospital stay, lower costs, less postoperative pain, and lower complication rates. While operative blood loss has been a major concern with laparoscopic resection, a number of reports is showing that minimally invasive approach is associated with lower risk of bleeding and transfusions. Tumor size is no longer an obstacle to laparoscopic resection, although laparoscopic major hepatectomy is still limited to experienced centers. The disadvantages of the laparoscopic approach are the loss of tactile sensation and palpation of the liver as well as the learning curve that is associated with laparoscopic resection. It should be noted that there has been no randomized clinical trials involving laparoscopic liver resection for malignancy and such trial is needed to clarify the risks vs benefits and help standardize the approach.

COMMENTS
Background

After being initially described for small peripheral benign tumors, laparoscopic liver resection for malignant and larger lesions is now reported extensively in the literature.

Research frontiers

This purpose of this study is to review the published literature on laparoscopic liver resection for malignant lesions. Authors discuss the different type of resection, the most common as well as the innovative techniques, the surgical outcomes, postoperative complications, and oncologic results.

Innovations and breakthroughs

Although laparoscopic liver surgery requires a great deal of experience by hepatobiliary surgeons, this approach is deemed safe for malignant liver lesions with comparable oncological results to open surgery.

Peer review

This manuscript thoroughly reviews the history and advances on the laparoscopic resection for liver malignancy, including the indications and contraindications, minor and major resections, hand-assisted technique, robotic resection, operative technical details, and the outcomes. The text is generally well written.

Footnotes

P- Reviewer: Actis GC, Geller DA, Li LQ, Perse M, Shi XY S- Editor: Wen LL L- Editor: A E- Editor: Zhang DN

References
1.  Gagner M, Rheault M, Dubuc J. Laparoscopic partial hepatectomy for liver tumor. Surg Endosc. 1993;6:99.  [PubMed]  [DOI]
2.  Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg. 2009;250:831-841.  [PubMed]  [DOI]
3.  Dagher I, O’Rourke N, Geller DA, Cherqui D, Belli G, Gamblin TC, Lainas P, Laurent A, Nguyen KT, Marvin MR. Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg. 2009;250:856-860.  [PubMed]  [DOI]
4.  Cho JY, Han HS, Yoon YS, Shin SH. Outcomes of laparoscopic liver resection for lesions located in the right side of the liver. Arch Surg. 2009;144:25-29.  [PubMed]  [DOI]
5.  Martin RC, Scoggins CR, McMasters KM. Laparoscopic hepatic lobectomy: advantages of a minimally invasive approach. J Am Coll Surg. 2010;210:627-634, 634-636.  [PubMed]  [DOI]
6.  Topal B, Fieuws S, Aerts R, Vandeweyer H, Penninckx F. Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc. 2008;22:2208-2213.  [PubMed]  [DOI]
7.  O’Rourke N, Shaw I, Nathanson L, Martin I, Fielding G. Laparoscopic resection of hepatic colorectal metastases. HPB (Oxford). 2004;6:230-235.  [PubMed]  [DOI]
8.  Yoon YS, Han HS, Cho JY, Ahn KS. Total laparoscopic liver resection for hepatocellular carcinoma located in all segments of the liver. Surg Endosc. 2010;24:1630-1637.  [PubMed]  [DOI]
9.  Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B. Laparoscopic liver resection. Br J Surg. 2006;93:67-72.  [PubMed]  [DOI]
10.  Mala T, Edwin B, Rosseland AR, Gladhaug I, Fosse E, Mathisen O. Laparoscopic liver resection: experience of 53 procedures at a single center. J Hepatobiliary Pancreat Surg. 2005;12:298-303.  [PubMed]  [DOI]
11.  Robles R, Marín C, Parrilla P. Laparoscopic liver resection for metastatic disease. Minerva Chir. 2008;63:441-453.  [PubMed]  [DOI]
12.  Kaneko H. Laparoscopic hepatectomy: indications and outcomes. J Hepatobiliary Pancreat Surg. 2005;12:438-443.  [PubMed]  [DOI]
13.  Abu Hilal M, Di Fabio F, Abu Salameh M, Pearce NW. Oncological efficiency analysis of laparoscopic liver resection for primary and metastatic cancer: a single-center UK experience. Arch Surg. 2012;147:42-48.  [PubMed]  [DOI]
14.  Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B. Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg. 2009;250:849-855.  [PubMed]  [DOI]
15.  Cugat E, Pérez-Romero N, Rotellar F, Suárez MA, Gastaca M, Artigas V, Olsina JJ, Noguera J, Martínez S, Moreno-Sanz C. Laparoscopic liver surgery: 8 years of multicenter Spanish register. J Hepatobiliary Pancreat Sci. 2010;17:262-268.  [PubMed]  [DOI]
16.  Bryant R, Laurent A, Tayar C, Cherqui D. Laparoscopic liver resection-understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg. 2009;250:103-111.  [PubMed]  [DOI]
17.  Buell JF, Thomas MT, Rudich S, Marvin M, Nagubandi R, Ravindra KV, Brock G, McMasters KM. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg. 2008;248:475-486.  [PubMed]  [DOI]
18.  Cai XJ, Yang J, Yu H, Liang X, Wang YF, Zhu ZY, Peng SY. Clinical study of laparoscopic versus open hepatectomy for malignant liver tumors. Surg Endosc. 2008;22:2350-2356.  [PubMed]  [DOI]
19.  Mostaedi R, Milosevic Z, Han HS, Khatri VP. Laparoscopic liver resection: Current role and limitations. World J Gastrointest Oncol. 2012;4:187-192.  [PubMed]  [DOI]
20.  Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg. 2009;250:825-830.  [PubMed]  [DOI]
21.  Gumbs AA, Tsai TJ, Hoffman JP. Initial experience with laparoscopic hepatic resection at a comprehensive cancer center. Surg Endosc. 2012;26:480-487.  [PubMed]  [DOI]
22.  Hompes D, Aerts R, Penninckx F, Topal B. Laparoscopic liver resection using radiofrequency coagulation. Surg Endosc. 2007;21:175-180.  [PubMed]  [DOI]
23.  Choi NK, Kim KH, Jung DH, Yu YD, Jung SW, Namkoong JM, Yoon SY, Lee SG. Laparoscopic liver resection for hepatocellular carcinoma: a three-year study of 57 Patients. Hepatogastroenterology. 2013;60:144-148.  [PubMed]  [DOI]
24.  Topal B, Tiek J, Fieuws S, Aerts R, Van Cutsem E, Roskams T, Prenen H. Minimally invasive liver surgery for metastases from colorectal cancer: oncologic outcome and prognostic factors. Surg Endosc. 2012;26:2288-2298.  [PubMed]  [DOI]
25.  Yoon YS, Han HS, Cho JY, Yoon CJ, Kim JH. Laparoscopic approach for treatment of multiple hepatocellular carcinomas. Surg Endosc. 2012;26:3133-3140.  [PubMed]  [DOI]
26.  Cannon RM, Scoggins CR, Callender GG, McMasters KM, Martin RC. Laparoscopic versus open resection of hepatic colorectal metastases. Surgery. 2012;152:567-573; discussion 573-574.  [PubMed]  [DOI]
27.  Ikeda T, Mano Y, Morita K, Hashimoto N, Kayashima H, Masuda A, Ikegami T, Yoshizumi T, Shirabe K, Maehara Y. Pure laparoscopic hepatectomy in semiprone position for right hepatic major resection. J Hepatobiliary Pancreat Sci. 2013;20:145-150.  [PubMed]  [DOI]
28.  Dagher I, Belli G, Fantini C, Laurent A, Tayar C, Lainas P, Tranchart H, Franco D, Cherqui D. Laparoscopic hepatectomy for hepatocellular carcinoma: a European experience. J Am Coll Surg. 2010;211:16-23.  [PubMed]  [DOI]
29.  Shafaee Z, Kazaryan AM, Marvin MR, Cannon R, Buell JF, Edwin B, Gayet B. Is laparoscopic repeat hepatectomy feasible? A tri-institutional analysis. J Am Coll Surg. 2011;212:171-179.  [PubMed]  [DOI]
30.  Lai EC, Tang CN, Yang GP, Li MK. Multimodality laparoscopic liver resection for hepatic malignancy--from conventional total laparoscopic approach to robot-assisted laparoscopic approach. Int J Surg. 2011;9:324-328.  [PubMed]  [DOI]
31.  Belli G, Fantini C, Belli A, Limongelli P. Laparoscopic liver resection for hepatocellular carcinoma in cirrhosis: long-term outcomes. Dig Surg. 2011;28:134-140.  [PubMed]  [DOI]
32.  Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S, Leteurtre E, Zerbib P, Pruvot FR. Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc. 2011;25:3668-3677.  [PubMed]  [DOI]
33.  Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P. Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg. 2011;35:2268-2274.  [PubMed]  [DOI]
34.  Hu BS, Chen K, Tan HM, Ding XM, Tan JW. Comparison of laparoscopic vs open liver lobectomy (segmentectomy) for hepatocellular carcinoma. World J Gastroenterol. 2011;17:4725-4728.  [PubMed]  [DOI]
35.  Kazaryan AM, Røsok BI, Marangos IP, Rosseland AR, Edwin B. Comparative evaluation of laparoscopic liver resection for posterosuperior and anterolateral segments. Surg Endosc. 2011;25:3881-3889.  [PubMed]  [DOI]
36.  Tranchart H, Diop PS, Lainas P, Pourcher G, Catherine L, Franco D, Dagher I. Laparoscopic major hepatectomy can be safely performed with colorectal surgery for synchronous colorectal liver metastasis. HPB (Oxford). 2011;13:46-50.  [PubMed]  [DOI]
37.  Sasaki A, Nitta H, Otsuka K, Takahara T, Nishizuka S, Wakabayashi G. Ten-year experience of totally laparoscopic liver resection in a single institution. Br J Surg. 2009;96:274-279.  [PubMed]  [DOI]
38.  Inagaki H, Kurokawa T, Yokoyama T, Ito N, Yokoyama Y, Nonami T. Results of laparoscopic liver resection: retrospective study of 68 patients. J Hepatobiliary Pancreat Surg. 2009;16:64-68.  [PubMed]  [DOI]
39.  Huang MT, Wei PL, Wang W, Li CJ, Lee YC, Wu CH. A series of laparoscopic liver resections with or without HALS in patients with hepatic tumors. J Gastrointest Surg. 2009;13:896-906.  [PubMed]  [DOI]
40.  Otsuka Y, Tsuchiya M, Maeda T, Katagiri T, Isii J, Tamura A, Yamazaki K, Kubota Y, Suzuki T, Suzuki T. Laparoscopic hepatectomy for liver tumors: proposals for standardization. J Hepatobiliary Pancreat Surg. 2009;16:720-725.  [PubMed]  [DOI]
41.  Zhang L, Chen YJ, Shang CZ, Zhang HW, Huang ZJ. Total laparoscopic liver resection in 78 patients. World J Gastroenterol. 2009;15:5727-5731.  [PubMed]  [DOI]
42.  Cho JY, Han HS, Yoon YS, Shin SH. Feasibility of laparoscopic liver resection for tumors located in the posterosuperior segments of the liver, with a special reference to overcoming current limitations on tumor location. Surgery. 2008;144:32-38.  [PubMed]  [DOI]
43.  Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA. Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg. 2011;146:348-356.  [PubMed]  [DOI]
44.  Azagra JS, Goergen M, Gilbart E, Jacobs D. Laparoscopic anatomical (hepatic) left lateral segmentectomy-technical aspects. Surg Endosc. 1996;10:758-761.  [PubMed]  [DOI]
45.  Inagaki H, Kurokawa T, Nonami T, Sakamoto J. Hand-assisted laparoscopic left lateral segmentectomy of the liver for hepatocellular carcinoma with cirrhosis. J Hepatobiliary Pancreat Surg. 2003;10:295-298.  [PubMed]  [DOI]
46.  Hüscher CG, Lirici MM, Chiodini S. Laparoscopic liver resections. Semin Laparosc Surg. 1998;5:204-210.  [PubMed]  [DOI]
47.  Dagher I, Proske JM, Carloni A, Richa H, Tranchart H, Franco D. Laparoscopic liver resection: results for 70 patients. Surg Endosc. 2007;21:619-624.  [PubMed]  [DOI]
48.  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;246:385-392; discussion 392-394.  [PubMed]  [DOI]
49.  Gumbs AA, Gayet B. Multimedia article. Totally laparoscopic extended right hepatectomy. Surg Endosc. 2008;22:2076-2077.  [PubMed]  [DOI]
50.  Gumbs AA, Bar-Zakai B, Gayet B. Totally laparoscopic extended left hepatectomy. J Gastrointest Surg. 2008;12:1152.  [PubMed]  [DOI]
51.  Abu Hilal M, Badran A, Di Fabio F, Pearce NW. Pure laparoscopic en bloc left hemihepatectomy and caudate lobe resection in patients with intrahepatic cholangiocarcinoma. J Laparoendosc Adv Surg Tech A. 2011;21:845-849.  [PubMed]  [DOI]
52.  Hu M, Zhao G, Xu D, Ma X, Liu R. Retroperitoneal laparoscopic hepatectomy: a novel approach. Surg Laparosc Endosc Percutan Tech. 2011;21:e245-e248.  [PubMed]  [DOI]
53.  Chen HY, Juan CC, Ker CG. Laparoscopic liver surgery for patients with hepatocellular carcinoma. Ann Surg Oncol. 2008;15:800-806.  [PubMed]  [DOI]
54.  Dagher I, Lainas P, Carloni A, Caillard C, Champault A, Smadja C, Franco D. Laparoscopic liver resection for hepatocellular carcinoma. Surg Endosc. 2008;22:372-378.  [PubMed]  [DOI]
55.  Ho CM, Wakabayashi G, Nitta H, Ito N, Hasegawa Y, Takahara T. Systematic review of robotic liver resection. Surg Endosc. 2013;27:732-739.  [PubMed]  [DOI]
56.  Giulianotti PC, Coratti A, Sbrana F, Addeo P, Bianco FM, Buchs NC, Annechiarico M, Benedetti E. Robotic liver surgery: results for 70 resections. Surgery. 2011;149:29-39.  [PubMed]  [DOI]
57.  Daouadi M, Zureikat AH, Zenati MS, Choudry H, Tsung A, Bartlett DL, Hughes SJ, Lee KK, Moser AJ, Zeh HJ. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg. 2013;257:128-132.  [PubMed]  [DOI]
58.  Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D, Dagher I. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc. 2010;24:1170-1176.  [PubMed]  [DOI]
59.  Gigot JF, Glineur D, Santiago Azagra J, Goergen M, Ceuterick M, Morino M, Etienne J, Marescaux J, Mutter D, van Krunckelsven L. Laparoscopic liver resection for malignant liver tumors: preliminary results of a multicenter European study. Ann Surg. 2002;236:90-97.  [PubMed]  [DOI]
60.  Belli G, Fantini C, D’Agostino A, Cioffi L, Langella S, Russolillo N, Belli A. Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc. 2007;21:2004-2011.  [PubMed]  [DOI]
61.  Abu Hilal M, Underwood T, Zuccaro M, Primrose J, Pearce N. Short- and medium-term results of totally laparoscopic resection for colorectal liver metastases. Br J Surg. 2010;97:927-933.  [PubMed]  [DOI]
62.  Nguyen KT, Laurent A, Dagher I, Geller DA, Steel J, Thomas MT, Marvin M, Ravindra KV, Mejia A, Lainas P. Minimally invasive liver resection for metastatic colorectal cancer: a multi-institutional, international report of safety, feasibility, and early outcomes. Ann Surg. 2009;250:842-848.  [PubMed]  [DOI]
63.  Guerron AD, Aliyev S, Agcaoglu O, Aksoy E, Taskin HE, Aucejo F, Miller C, Fung J, Berber E. Laparoscopic versus open resection of colorectal liver metastasis. Surg Endosc. 2013;27:1138-1143.  [PubMed]  [DOI]