Systematic Reviews Open Access
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World J Gastroenterol. Dec 14, 2014; 20(46): 17595-17602
Published online Dec 14, 2014. doi: 10.3748/wjg.v20.i46.17595
Costs of laparoscopic and open liver and pancreatic resection: A systematic review
Paolo Limongelli, Chiara Vitiello, Salvatore Tolone, Gianmattia del Genio, Luigi Brusciano, Giovanni Docimo, Ludovico Docimo, XI Division of General and Obesity Surgery, Second University of Naples, 80131 Naples, Italy
Andrea Belli, Division of Surgical Oncology D, National Cancer Institute of Naples, Fondazione G. Pascale, 80131 Naples, Italy
Madhava Pai, Nagy Habib, Long Richard Jiao, Department of Surgery and Cancer, HPB Surgical Unit, Imperial College, Hammersmith Hospital Campus, London W12 0HS, United Kingdom
Giulio Belli, Department of General and Hepato-Pancreato-Biliary Surgery, S.M. Loreto Nuovo Hospital, 80142 Naples, Italy
Author contributions: Limongelli P and Vitiello C contributed to conception, design and drafting of the article; Belli A, Pai M, Tolone S, del Genio G, Brusciano and Docimo G contributed to acquisition and interpretation of data; Habib N, Belli G, Jiao LR and Docimo L revised it critically and gave final approval of the version to be published.
Correspondence to: Paolo Limongelli, MD, PhD, XI Division of General and Obesity Surgery, Second University of Naples, Via Pansini 5, 80131 Naples, Italy. paolo.limongelli@unina2.it
Telephone: +39-81-5666237 Fax: +39-81-5666669
Received: March 5, 2014
Revised: April 20, 2014
Accepted: May 26, 2014
Published online: December 14, 2014
Processing time: 288 Days and 10.1 Hours

Abstract

AIM: To study costs of laparoscopic and open liver and pancreatic resections, all the compiled data from available observational studies were systematically reviewed.

METHODS: A systematic review of the literature was performed using the Medline, Embase, PubMed, and Cochrane databases to identify all studies published up to 2013 that compared laparoscopic and open liver [laparoscopic hepatic resection (LLR) vs open liver resection (OLR)] and pancreatic [laparoscopic pancreatic resection (LPR) vs open pancreatic resection] resection. The last search was conducted on October 30, 2013.

RESULTS: Four studies reported that LLR was associated with lower ward stay cost than OLR (2972 USD vs 5291 USD). The costs related to equipment (3345 USD vs 2207 USD) and theatre (14538 vs 11406) were reported higher for LLR. The total cost was lower in patients managed by LLR (19269 USD) compared to OLR (23419 USD). Four studies reported that LPR was associated with lower ward stay cost than OLR (6755 vs 9826 USD). The costs related to equipment (2496 USD vs 1630 USD) and theatre (5563 vs 4444) were reported higher for LPR. The total cost was lower in the LPR (8825 USD) compared to OLR (13380 USD).

CONCLUSION: This systematic review support the economic advantage of laparoscopic over open approach to liver and pancreatic resection.

Key Words: Hepatobiliary resection; Laparoscopic hepatic resection; Open liver resection; Laparoscopic pancreatic resection; Open pancreatic resection

Core tip: Laparoscopic hepatobiliary and pancreatic surgery has progressed over the last years but has been slow to gain widespread acceptance even in some referral centers worldwide. Cost implications of a mini-invasive approach to hepatobiliary and pancreatic surgery are still unknown. A systematic review of the literature was performed. The total cost was lower in patients managed by laparoscopic liver resection. The total cost was lower in the laparoscopic pancreatic resection than in open pancreatic resection. This systematic review support the economic advantage of laparoscopic over open approach to liver and pancreatic resection.



INTRODUCTION

Laparoscopic hepatobiliary and pancreatic (HPB) surgery has undergone a consistent evolution and a progressive diffusion over the last decade, though it may be complex, technically demanding and requires specific high surgical skills[1]. Despite technical challenges, laparoscopic liver surgery has been widely reported with minor and major resections performed for benign and malignant lesions even in cirrhotic patients[2-9]. Although prospective randomized trials are lacking, the laparoscopic approach to liver resection seems to warrant reduced overall morbidity rate and comparable oncological outcomes than the open approach[10-12]. On the other hand, the progression of laparoscopic pancreatic surgery has been relatively slow among traditional surgeons, with only few emerging specialty centers reporting excellent outcomes for advanced and complex operations, such as laparoscopic pancreaticoduodenectomy (LPD)[13-15]. Whereas LPD should still be considered in its learning curve, due to longer operation time and complicated reconstruction steps, laparoscopic distal pancreatectomy (LDP) has been largely compared with the open approach in literature so far. A recent review, suggested that the mini-invasive approach is associated with lower risk of overall postoperative complications and wound infection, no substantial increase in the operative time, and with a comparable rate of positive resection margin[16]. Despite the above mentioned advantages, the laparoscopic approach to HPB surgery has been slow to gain widespread acceptance even in some referral centers worldwide. Multifactorial reasons to explain this exist, but one that may play an important role is related to the unknown cost implications of a mini-invasive approach to HPB surgical interventions. The systematic reviews and/or meta-analyses published so far have analyzed either short- and long-term results of open versus laparoscopic HPB surgery without focusing on cost-effectiveness[17,18]. The present systematic review of the literature compared costs of laparoscopic and open surgical treatment for liver and pancreatic resection, addressing direct and indirect costs.

MATERIALS AND METHODS
Study selection

A systematic review of the literature was performed using the Medline, Embase, PubMed, and Cochrane databases to identify all studies published form 1987 up to 2013 that compared laparoscopic and open liver and pancreatic resection. This study was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines[19]. The following medical subject heading (MeSH) terms and key words were used: “laparoscopy,”“minimally invasive surgery,”“laparotomy,”“hepatectomy,”“liver resection,”“open liver resection (OLR),”“hepatic resection,”“laparoscopic liver resection,”“segmentectomy,”“sectionectomy,”“treatment outcome,” and “wedge resections”, “pancreatectomy,” pancreatoduodenectomy, distal pancreatectomy, “open pancreatic resection,”“laparoscopic pancreatic resection,” and “comparative study”. Furthermore, the combinations of these terms were used. The term “vs” was used to find comparative studies. All the searched abstracts, studies, and citations were analyzed. All the potential articles were cross-referenced. The related article’s function was used to broaden the search, and all abstracts, studies, and citations obtained were reviewed. References of the articles acquired were also searched by hand. The last search was conducted on October 30, 2013.

Data extraction

Each study was independently evaluated by 2 reviewers (P.L. and C.V.) for inclusion or exclusion from the review and the following data was extracted: first author, year of publication, characteristics of study population, study design, indications for surgery, matching criteria, number of subjects operated with each technique and direct and indirect costs.

Inclusion criteria

To enter our analysis, studies had to fulfill the following: (1) comparison of costs of laparoscopic (with or without hand-assisted technique) to open approaches in patients undergoing liver and pancreatic resection; (2) objective evaluation of at least one of the outcome measures mentioned below; and (3) when 2 studies were reported by the same institution (and/or authors), either the study with the larger sample size or the one of higher quality was included. However, this was not applicable if the outcome measures were mutually exclusive or measured at different time intervals.

Exclusion criteria

Studies that failed to fulfill the inclusion criteria were excluded. In addition, the following criteria were used to exclude studies: (1) studies in which the outcome of interest mentioned below were not reported or if it was impossible to calculate these from the published reports; (2) studies that focused on other laparoscopic hepatobiliary and pancreatic operations rather than elective resection benign and malignant lesions; (3) studies involving exclusively robotic procedures. However, we included the conventional laparoscopic and open data, if presented by the same group and/or reported in the same study; and (4) studies written in languages other than English.

Assessment of methodological quality

The methodological quality of the studies was assessed independently by two authors. All studies were graded according to the Oxford Centre for Evidence-Based Medicine (CEBM) levels of evidence[20]. The risk of bias was assessed using a standardized list of ten potential risks of bias, based on the Oxford CEBM Critical Appraisal Skills Programme appraisal sheets for economic evaluation studies[21].

Outcomes of interest and definitions

Laparoscopic and open approaches to HPB surgery were compared on the basis of cost effectiveness analysis. Liver resections were defined according to the Brisbane 2000 classification[22]: minor (two or fewer segments) or major (at least three segments) according to Couinaud’s classification. Cost analysis included theatre costs, equips and equipment costs, nursing, blood transfusion requirement, laboratory testing, postoperative imaging, any re-intervention (radiological and/or surgical) and overall hospital stay. In addition, the cost for readmission from discharge including any associated re-intervention (radiological and/or surgical) and new hospital stay were reviewed. The direct cost of the operation, the direct cost of the postoperative hospital period and the total cost with and without readmission and intervention was analyzed both separately and together. Since most of the data were expressed in US dollars (USD), the remaining were converted to this currency using up to date exchange rates.

Statistical analysis

Mean ± SD or median (range) values were extracted from articles or obtained from the study authors if necessary. Weighted mean ± SD values were calculated using the mean ± SD values reported in the individual studies, or those derived from median (range) values using the methods described by Hozo et al[23]. Cost analysis included operative time and supplies, anesthesia, nursing, laboratory, and overall hospital stay costs. The direct cost of operation, as well as the direct cost of the entire associated hospital stay was calculated.

RESULTS

There were total of 15 studies that compared operative costs between laparoscopic and open hepatic and pancreatic resection for benign and/or malignant lesions. Nine studies compared costs between laparoscopic (344/682) and open (338/682) hepatic resection (LLR vs OLR)[24-32].

Whereas six studies[33-38] focused on costs differences between laparoscopic (249/495) and open (246/495) pancreatic resection (LPR vs OPR). Studies were carried out from different countries all over the word with eight of them reporting figures expressed in USD. The other currencies used to express data in the other studies (pound in 3; Euros in 2; Canadian dollars in 1; South Korean WOW in 1), were converted to USD. Twelve out of fifteen studies were retrospective, with only three reported as prospective cohort studies. All were conducted in a year interval ranging from a minimum of 3 to a maximum of 11 years and on a total number of patients ranging from 30 to 144 patients (Table 1).

Table 1 Study characteristics.
Ref.YearCountryStudy designSample sizeStudy interval (yr)Study population
Polignano et al[24]2008United KingdomNon-randomised prospective cohort502Liver resection
Tsinberg et al[25]2009United StatesNon-randomised prospective cohort3410Liver resection
Rowe et al[26]2009United StatesNon-randomised prospective cohort303Liver resection
Vanounou et al[27]2010United StatesRetrospective cohort736Liver resection
Nguyen et al[28]2011United StatesRetrospective cohort769Liver resection
Bhojani et al[29]2011CanadaRetrospective cohort1444Liver resection
Stoot et al[30]2012NetherlandsRetrospective cohort287Liver resection
Abu Hilal et al[31]2013United KingdomRetrospective cohort1497Liver resection
Cannon et al[32]2013United StatesRetrospective cohort984Liver resection
Kim et al[33]2008South CoreaRetrospective cohort128-Pancreatic resection
Eom et al[34]2008South CoreaRetrospective cohort9311Pancreatic resection
Waters et al[35]2010United StatesRetrospective cohort601Pancreatic resection
Fox et al[36]2008CanadaRetrospective cohort1186Pancreatic resection
Abu Hilal et al[37]2012United KingdomRetrospective cohort516Pancreatic resection
Limongelli et al[38]2012ItalyRetrospective cohort4510Pancreatic resection
Methodological quality

Details of the methodological quality of the included studies are shown in Table 2. All the studies provided evidence that the effects of the intervention were measured and valued appropriately.

Table 2 Assessment of methodological quality.
Ref.Level of evidenceMeasurements accuracyDiscountingSensitivity analysisTranslatability to other setting
Polignano et al[24]3-
Tsinberg et al[25]3-
Rowe et al[26]3-
Vanounou et al[27]4-
Nguyen et al[28]4-
Bhojani et al[29]3-
Stoot et al[30]3-
Abu Hilal et al[31]3-
Cannon et al[32]4-
Kim et al[33]4-
Eom et al[34]4-
Waters et al[35]4-
Fox et al[36]4-
Abu Hilal et al[37]4-
Limongelli et al[38]4-

In none of the studies an analysis of costs and consequences adjusted for different times at which they occurred (discounting) was applicable. A sensitivity analysis was conducted only in one study[35]. Despite the peculiarity of each patient population and setting where the studies were carried out, the costs appeared to be partly translatable to other settings.

Liver resection

Four studies[24,29-31] reported that LLR was associated with lower ward stay cost than OLR (2972 USD vs 5291 USD). This trend concerning hospital costs was confirmed also for High Dependency Unit and Postoperative Anestesia Care Unit (HDU/PACU) that resulted more expensive in patients undergoing OLR (5857 USD vs 1829 USD) (Table 3)[24,29,31]. On the contrary, costs related to operation were higher in the group of patients undergoing LLR. Specifically both equipment (3345 USD vs 2207 USD) and theatre (14538 vs 11406) costs were reported higher for LLR respectively by four[24,26,30,31] and six studies[24,25,31,32]. The total cost was lower in patients managed by LLR (19269 USD) compared to OLR (23419 USD). By analyzing a subset of six[24,25,27,29-31] studies exclusively focused on outcome of minor laparoscopic resection, the total cost of LLR was lower (12720 USD) compared to OLR (17429 USD).

Table 3 Hospital and operative costs of laparoscopic hepatic resection vs open liver resection.
Ref. (n)Ward stayHDU/PACUEquipmentTheatreTotal costs
Polignano et al[24] (50)
LLR (25)5535 ± 25761558 ± 19402302 ± 76911539 ± 378920739 ± 5814
OLR (25)8306 ± 55674178± 18781041 ± 66811755 ± 235325285 ± 6750
Tsinberg et al[25] (34)
LLR (18)---28900 ± 211836784 ± 3505
OLR (16)--28023 ± 224747358 ± 3717
Rowe et al[26] (30)
LLR (18)--1071 ± 345--
OLR (12)--851 ± 424--
Vanounou et al[27] (73) 1
LLR (44)----17290
OLR (29)----13962
Nguyen et al[28] (76)2
LLR (34)---1.301.87
OLR (42)---1.001.92
Bhojani et al[29] (144)1
OLR (94)3647652-359811376
LLR (50)5215641-396412523
Stoot et al[30] (28)
OLR (14)2014 ± 510-2113 ± 4873038 ± 7437167 ± 1335
LLR (14)1957 ± 599-2360 ± 3373583 ± 7947901 ± 1107
Abu Hilal et al[31] (149)1
LLR (LRH)(38)238542495579108467139
OLR (ORH)(46)523290222981721018222
OLR (OLLS)(19)173434523947485220579
LLR (LLLS)(46)430019182613655714252
Cannon et al[32] (98)1
OLR (41)---3401949993
LLR (57)---3140054703
Overall studies6062
LLR (310) 22972182935451453819269
OLR (296) 25291585722071140623419
Pancreatic resection

Four studies[35-38] reported that LPR was associated with lower ward stay cost than OLR (6755 USD vs 9826 USD). No studies specifically reported on HDU/PACU costs after either LPR or OPR (Table 4). On the contrary, costs related to operation were higher in the group of patients undergoing LPR. Specifically both equipment (2496 USD vs 1630 USD) and theatre (5563 vs 4444) costs were reported higher for LPR respectively by one[38] and four studies[35-38]. The total cost was lower in the LPR (8825 USD) compared to OLR (13380 USD).

Table 4 Hospital and operative costs of laparoscopic pancreatic resection vs open pancreatic resection.
Ref. (n)Ward stayHDU/PACUEquipmentTheatreTotal costs
Kim et al[33] (128)
LPR (93)----4745 ± 1481
OPR (35)----4953 ± 3437
Eom et al[34] (31)
LPR (18)----4884 ± 1845
OPR (13)---3401 ± 1247
Waters et al[35] (60) 1
LPR (32)9828--307212900
OPR (28)12011--351015521
Fox et al[36] (118) 1
LPR (42)3404--465510842
OPR (76)5462--451013656
Abu Hilal et al[37] (51) 1
LPR (35)7446--988917337
OPR (16)25441--949834937
Limongelli et al[38] (45)
LPR (16)7894 ± 1771-2496 ± 1273469 ± 12611531 ± 1918
OPR (29)10540 ± 3230-1630 ± 3292388 ± 36113141 ± 3631
Overall (495)
LPR (249)6755-249655638825
OPR (246)9826-1630444413380
DISCUSSION

This systematic review has compared the costs of laparoscopic and open approach to HPB resection and analyzed methodological quality of the studies. Laparoscopic liver resection was associated with higher costs related to equipment and theatre. On the other hand, LLR carried less expensive hospital costs, such as ward costs and peri-operative care. Specifically the costs of HDU and PACU resulted higher in OLR. Finally, when analyzing the total cost of the procedure, the economic advantage for LLR was greater than that for OLR. Laparoscopic pancreatic resection was associated with higher costs related to equipment and theatre. On the other hand, OPR was associated with higher hospital stay cost, such as ward costs, but no studies specifically reported data on costs related to HDU or PACU utilization after LPR or OPR. At last, the total cost of the procedure resulted higher for the group of patients undergoing OPR compared to those treated by LPR. This study is the one of the systematic review to be conducted that specifically compared costs of laparoscopic and open HPB resections. To our knowledge, there has been no randomized controlled trial or systemic review evaluating this topic before. This study included 9 observational studies comparing costs between laparoscopic and open hepatic resection. All studies with an overall participants’ size of 601 patients were retrospectively conducted, with only 2 of them reported as prospective comparisons[25,26]. The inclusion and exclusion criteria of majority of the studies were clearly stated, with most studies having laparoscopic and open resection matched for demographics and characteristics of the patients. None of the studies but one assess the financial implications of laparoscopy for major and minor liver resections[31]. Authors supported the cost advantage of left lateral sectionectomy (LLS), one of the most performed minor LLR. On the other hand they showed cost neutrality of laparoscopic compared to open right liver resection, suggesting that protocols of enhanced recovery after surgery would be likely to reduce costs of both OLR and LLR. In the present study, by analyzing a subset of six studies reporting only data on minor liver resection we found economic advantages in terms of total cost in the group of patients undergoing LLR than OLR.

Concerning pancreatic resections, we found no specific studies comparing laparoscopic versus open pancreaticoduodenectomy that still represents an uncommon indication to laparoscopic approach, and is still performed in few surgical centers worldwide. On the contrary, LDP seems to carry advantages related to minimal-access surgery, such as reduced postoperative pain, faster recovery, wound complications, lower intraoperative blood loss and fewer postoperative complications[39]. So far, six studies have compared costs between laparoscopic and open distal pancreatic resections (LPR vs OPR) and all were retrospective cohorts with a total of 433 patients. Each study had laparoscopic and open resections unmatched for demographics and characteristics of the patients except one who designed a case control comparison with a 2:1 matching[34]. One of the studies also compared the direct cost of operation and of the entire associated hospital stay between OPR, LPR and robotic distal pancreatectomy. Authors showed operative and postoperative costs were similar among all groups, indicating robotic distal pancreatectomy to be safe and cost effective in selected cases. There are some limitations that must be taken into account when interpreting the results of the current analysis. First, by grading down the level of the studies on the basis of study quality, it is clear this systematic review could include only studies of poor-moderate quality. Moreover, we choose not to perform a sensitivity analysis to evaluate the impact of methodological quality on the operative and hospital costs of laparoscopic and open liver and pancreatic resection. This was because of lack of data from studies of the highest quality, defined by a level of evidence of 1 and 2. Confounding by indication was a common risk of bias in most cohort studies because related to the choice of approach merely based on surgeon’s clinical judgment. Specifically, due to the severe heterogeneity of liver resection data collected in this analysis, it is safe to assume that centers would have chosen LLR for minor and uncomplicated cases and OLR for major and complicated cases. Despite the peculiarity of each patient population and setting where the studies were carried out, the methodological evaluation costs appeared to be in part translatable to other settings. However, the economic parameters used in the assessment are likely to differ from country to country, based on the type of healthcare and reimbursement system. In a recent study, a higher proportion of patients treated with LDP were readmitted to undergo interventional procedures after an initial shorter hospitalization[40]. Authors suggested that adding days spent in readmission to the initial length of hospital stay eliminates the perceived effect of the laparoscopic approach to pancreatic distal resection. The majority of studies included in this analysis did not assess and compare costs of laparoscopic and open liver and pancreatic resections before and after readmission to hospital. With respect to pancreatic resection, Fox et al[36] reported a major impact of pancreatic fistula on total hospital cost in the ODP cohort, but comparable in-hospital complications between LDP and ODP cohorts in terms of total hospital cost. In line with this figures, a recent study included in the present review showed the total cost of OLR and LPR were not significantly different after including patients readmission[37]. Among studies addressing comparative costs between OLR and LLR, two of them employed deviation-based cost modeling and weighted average mean cost. One study showed the overall cost savings per patient undergoing laparoscopic LLS was around three thousand dollars less that a patient undergoing a similar open operation[27]. This results were confirmed by Cannon and coworkers who showed an high average cost savings for patients undergoing LLR compared to those treated by OLR[32]. Authors did not find any advantages of laparoscopy in the subset of patients undergoing right hepatectomy, suggesting the benefit of laparoscopy is related to the difficulty of surgery, resulting into a compensation between higher operative costs and the financial benefits of a shorter and less complicated hospital stay. Whether this finding is due to the complexity of a laparoscopic approach associated with dramatic longer operative time or is the result of both higher morbidity and readmission rate after major LLR is still to be demonstrated.

In conclusion, this study summarized the available evidence on financial comparison between laparoscopic and open approach to liver and pancreatic resections including assessment of methodological quality, without an attempt at meta-analysis, as this would have been inappropriate given the heterogeneity in study designs and protocols.

COMMENT
Background

Laparoscopic hepatobiliary and pancreatic (HPB) surgery has undergone a consistent evolution and a progressive diffusion over the last decade, though it may be complex, technically demanding and requires specific high surgical skills.

Research frontiers

The present systematic review of the literature compared costs of laparoscopic and open surgical treatment for liver and pancreatic resection, addressing direct and indirect costs.

Innovations and breakthroughs

A systematic review of the literature was performed using the Medline, Embase, PubMed, and Cochrane databases to identify all studies published up to 2013 that compared laparoscopic and open liver and pancreatic resection.

Applications

This systematic review support the economic advantage of laparoscopic over open approach to liver and pancreatic resection.

Peer review

This study focused on the economical aspect of laparoscopic HPB for the first time in English review articles. This article is novel and well-described.

Footnotes

P- Reviewer: Anadol Z, Fabre JM, Hu H, Jani K, Ogiso S, Tsuchida A S- Editor: Ding Y L- Editor: A E- Editor: Zhang DN

References
1.  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]  [Cited in This Article: ]  [Cited by in Crossref: 1213]  [Cited by in F6Publishing: 1117]  [Article Influence: 74.5]  [Reference Citation Analysis (0)]
2.  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]  [Cited in This Article: ]  [Cited by in Crossref: 132]  [Cited by in F6Publishing: 143]  [Article Influence: 9.5]  [Reference Citation Analysis (0)]
3.  Belli G, Fantini C, D’Agostino A, Cioffi L, Limongelli P, Russo G, Belli A. Laparoscopic segment VI liver resection using a left lateral decubitus position: a personal modified technique. J Gastrointest Surg. 2008;12:2221-2226.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 21]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
4.  Kim KH, Jung DH, Park KM, Lee YJ, Kim DY, Kim KM, Lee SG. Comparison of open and laparoscopic live donor left lateral sectionectomy. Br J Surg. 2011;98:1302-1308.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 110]  [Cited by in F6Publishing: 109]  [Article Influence: 8.4]  [Reference Citation Analysis (0)]
5.  Cannon RM, Brock GN, Marvin MR, Buell JF. Laparoscopic liver resection: an examination of our first 300 patients. J Am Coll Surg. 2011;213:501-507.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 59]  [Cited by in F6Publishing: 56]  [Article Influence: 4.3]  [Reference Citation Analysis (0)]
6.  Kaneko H, Takagi S, Shiba T. Laparoscopic partial hepatectomy and left lateral segmentectomy: technique and results of a clinical series. Surgery. 1996;120:468-475.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 211]  [Cited by in F6Publishing: 205]  [Article Influence: 7.3]  [Reference Citation Analysis (0)]
7.  Koffron A, Geller D, Gamblin TC, Abecassis M. Laparoscopic liver surgery: Shifting the management of liver tumors. Hepatology. 2006;44:1694-1700.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 119]  [Cited by in F6Publishing: 123]  [Article Influence: 6.8]  [Reference Citation Analysis (0)]
8.  Belli G, Cioffi L, Fantini C, D’Agostino A, Russo G, Limongelli P, Belli A. Laparoscopic redo surgery for recurrent hepatocellular carcinoma in cirrhotic patients: feasibility, safety, and results. Surg Endosc. 2009;23:1807-1811.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 80]  [Cited by in F6Publishing: 72]  [Article Influence: 4.8]  [Reference Citation Analysis (0)]
9.  Tzanis D, Shivathirthan N, Laurent A, Abu Hilal M, Soubrane O, Kazaryan AM, Ettore GM, Van Dam RM, Lainas P, Tranchart H. European experience of laparoscopic major hepatectomy. J Hepatobiliary Pancreat Sci. 2013;20:120-124.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 73]  [Cited by in F6Publishing: 81]  [Article Influence: 7.4]  [Reference Citation Analysis (0)]
10.  Simillis C, Constantinides VA, Tekkis PP, Darzi A, Lovegrove R, Jiao L, Antoniou A. Laparoscopic versus open hepatic resections for benign and malignant neoplasms--a meta-analysis. Surgery. 2007;141:203-211.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 149]  [Cited by in F6Publishing: 125]  [Article Influence: 7.4]  [Reference Citation Analysis (0)]
11.  Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign and malignant tumors: An updated meta-analysis. Arch Surg. 2010;145:1109-1118.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 116]  [Cited by in F6Publishing: 114]  [Article Influence: 8.1]  [Reference Citation Analysis (0)]
12.  Rao A, Rao G, Ahmed I. Laparoscopic or open liver resection? Let systematic review decide it. Am J Surg. 2012;204:222-231.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 53]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
13.  Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, Souda H, Gunji H, Miyazaki A, Ikeda A. Comparison of laparoscopy-assisted and open pylorus-preserving pancreaticoduodenectomy for periampullary disease. Am J Surg. 2009;198:445-449.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 89]  [Cited by in F6Publishing: 98]  [Article Influence: 6.5]  [Reference Citation Analysis (0)]
14.  Kuroki T, Adachi T, Okamoto T, Kanematsu T. A non-randomized comparative study of laparoscopy-assisted pancreaticoduodenectomy and open pancreaticoduodenectomy. Hepatogastroenterology. 2012;59:570-573.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 63]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]
15.  Zureikat AH, Breaux JA, Steel JL, Hughes SJ. Can laparoscopic pancreaticoduodenectomy be safely implemented? J Gastrointest Surg. 2011;15:1151-1157.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 108]  [Cited by in F6Publishing: 121]  [Article Influence: 9.3]  [Reference Citation Analysis (0)]
16.  Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048-1059.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 374]  [Cited by in F6Publishing: 378]  [Article Influence: 31.5]  [Reference Citation Analysis (0)]
17.  Mirnezami R, Mirnezami AH, Chandrakumaran K, Abu Hilal M, Pearce NW, Primrose JN, Sutcliffe RP. Short- and long-term outcomes after laparoscopic and open hepatic resection: systematic review and meta-analysis. HPB (Oxford). 2011;13:295-308.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 158]  [Cited by in F6Publishing: 158]  [Article Influence: 12.2]  [Reference Citation Analysis (0)]
18.  Nakamura M, Nakashima H. Laparoscopic distal pancreatectomy and pancreatoduodenectomy: is it worthwhile? A meta-analysis of laparoscopic pancreatectomy. J Hepatobiliary Pancreat Sci. 2013;20:421-428.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 111]  [Cited by in F6Publishing: 108]  [Article Influence: 9.8]  [Reference Citation Analysis (0)]
19.  Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151:264-29, W64.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18463]  [Cited by in F6Publishing: 17464]  [Article Influence: 1164.3]  [Reference Citation Analysis (0)]
20.  Oxford Centre for Evidence-Based Medicine Levels of Evidence Working Group. The Oxford 2011 Levels of Evidence; 2011.  Available from: http://www.cebm.net/index.aspx?o=5653[accessed 23 November 2011].  [PubMed]  [DOI]  [Cited in This Article: ]
21.   Available from: http://www.casp-uk.net.  [PubMed]  [DOI]  [Cited in This Article: ]
22.  Pang YY. The Brisbane 2000 terminology of liver anatomy and resections. HPB 2000; 2: 333-39. HPB (Oxford). 2002;4:99; author reply 99-100.  [PubMed]  [DOI]  [Cited in This Article: ]
23.  Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol. 2005;5:13.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4895]  [Cited by in F6Publishing: 6518]  [Article Influence: 343.1]  [Reference Citation Analysis (0)]
24.  Polignano FM, Quyn AJ, de Figueiredo RS, Henderson NA, Kulli C, Tait IS. Laparoscopic versus open liver segmentectomy: prospective, case-matched, intention-to-treat analysis of clinical outcomes and cost effectiveness. Surg Endosc. 2008;22:2564-2570.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 130]  [Cited by in F6Publishing: 139]  [Article Influence: 8.7]  [Reference Citation Analysis (0)]
25.  Tsinberg M, Tellioglu G, Simpfendorfer CH, Walsh RM, Vogt D, Fung J, Berber E. Comparison of laparoscopic versus open liver tumor resection: a case-controlled study. Surg Endosc. 2009;23:847-853.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 90]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
26.  Rowe AJ, Meneghetti AT, Schumacher PA, Buczkowski AK, Scudamore CH, Panton ON, Chung SW. Perioperative analysis of laparoscopic versus open liver resection. Surg Endosc. 2009;23:1198-1203.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 40]  [Cited by in F6Publishing: 39]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
27.  Vanounou T, Steel JL, Nguyen KT, Tsung A, Marsh JW, Geller DA, Gamblin TC. Comparing the clinical and economic impact of laparoscopic versus open liver resection. Ann Surg Oncol. 2010;17:998-1009.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 121]  [Cited by in F6Publishing: 123]  [Article Influence: 8.2]  [Reference Citation Analysis (0)]
28.  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]  [Cited in This Article: ]  [Cited by in Crossref: 272]  [Cited by in F6Publishing: 282]  [Article Influence: 20.1]  [Reference Citation Analysis (0)]
29.  Bhojani FD, Fox A, Pitzul K, Gallinger S, Wei A, Moulton CA, Okrainec A, Cleary SP. Clinical and economic comparison of laparoscopic to open liver resections using a 2-to-1 matched pair analysis: an institutional experience. J Am Coll Surg. 2012;214:184-195.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 43]  [Cited by in F6Publishing: 38]  [Article Influence: 2.9]  [Reference Citation Analysis (0)]
30.  Stoot JH, van Dam RM, Coelen RJ, Winkens B, Olde Damink SW, Bemelmans MH, Dejong CH. The introduction of a laparoscopic liver surgery programme: a cost analysis of initial experience in a university hospital. Scand J Surg. 2012;101:32-37.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 79]  [Cited by in F6Publishing: 78]  [Article Influence: 5.2]  [Reference Citation Analysis (0)]
31.  Abu Hilal M, Di Fabio F, Syed S, Wiltshire R, Dimovska E, Turner D, Primrose JN, Pearce NW. Assessment of the financial implications for laparoscopic liver surgery: a single-centre UK cost analysis for minor and major hepatectomy. Surg Endosc. 2013;27:2542-2550.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 50]  [Cited by in F6Publishing: 51]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
32.  Cannon RM, Scoggins CR, Callender GG, Quillo A, McMasters KM, Martin RC. Financial comparison of laparoscopic versus open hepatic resection using deviation-based cost modeling. Ann Surg Oncol. 2013;20:2887-2892.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 35]  [Cited by in F6Publishing: 36]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
33.  Kim SC, Park KT, Hwang JW, Shin HC, Lee SS, Seo DW, Lee SK, Kim MH, Han DJ. Comparative analysis of clinical outcomes for laparoscopic distal pancreatic resection and open distal pancreatic resection at a single institution. Surg Endosc. 2008;22:2261-2268.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 137]  [Cited by in F6Publishing: 123]  [Article Influence: 7.7]  [Reference Citation Analysis (0)]
34.  Eom BW, Jang JY, Lee SE, Han HS, Yoon YS, Kim SW. Clinical outcomes compared between laparoscopic and open distal pancreatectomy. Surg Endosc. 2008;22:1334-1338.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 106]  [Cited by in F6Publishing: 116]  [Article Influence: 6.8]  [Reference Citation Analysis (0)]
35.  Waters JA, Canal DF, Wiebke EA, Dumas RP, Beane JD, Aguilar-Saavedra JR, Ball CG, House MG, Zyromski NJ, Nakeeb A. Robotic distal pancreatectomy: cost effective? Surgery. 2010;148:814-823.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 175]  [Cited by in F6Publishing: 178]  [Article Influence: 12.7]  [Reference Citation Analysis (0)]
36.  Fox AM, Pitzul K, Bhojani F, Kaplan M, Moulton CA, Wei AC, McGilvray I, Cleary S, Okrainec A. Comparison of outcomes and costs between laparoscopic distal pancreatectomy and open resection at a single center. Surg Endosc. 2012;26:1220-1230.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 64]  [Cited by in F6Publishing: 73]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
37.  Abu Hilal M, Hamdan M, Di Fabio F, Pearce NW, Johnson CD. Laparoscopic versus open distal pancreatectomy: a clinical and cost-effectiveness study. Surg Endosc. 2012;26:1670-1674.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 93]  [Cited by in F6Publishing: 101]  [Article Influence: 7.8]  [Reference Citation Analysis (0)]
38.  Limongelli P, Belli A, Russo G, Cioffi L, D’Agostino A, Fantini C, Belli G. Laparoscopic and open surgical treatment of left-sided pancreatic lesions: clinical outcomes and cost-effectiveness analysis. Surg Endosc. 2012;26:1830-1836.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 62]  [Cited by in F6Publishing: 70]  [Article Influence: 5.8]  [Reference Citation Analysis (0)]
39.  Briggs CD, Mann CD, Irving GR, Neal CP, Peterson M, Cameron IC, Berry DP. Systematic review of minimally invasive pancreatic resection. J Gastrointest Surg. 2009;13:1129-1137.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
40.  Baker MS, Bentrem DJ, Ujiki MB, Stocker S, Talamonti MS. Adding days spent in readmission to the initial postoperative length of stay limits the perceived benefit of laparoscopic distal pancreatectomy when compared with open distal pancreatectomy. Am J Surg. 2011;201:295-299; discussion 295-299.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 31]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]