Since the first laparoscopic liver resection (LLR) was reported in 1992 by Gagner et al. (1) at the Scientific Session of the Society of American Gastrointestinal Surgeons, minimally invasive techniques in liver surgery have continued to develop. LLR is worldwide accepted based on the excellent results shown over the years. The number of publications on LLR increase each year and so the citation index. LLR is certainly one of the fields with the greatest expansion in the scientific surgical community. Despite the fast-growing amount of data, it took 16 years before the first international position on laparoscopic liver surgery was released: The Louisville Statement in 2008 (2).
The present study identifies the 100 most-cited articles related to LLR, analyzes the trends in these articles according to publication year and summarizes on the knowledge and evidence these one-hundred articles brought to the surgical community.
We performed a search to identify all studies dealing with LLR by utilizing the Institute for Scientific Information (ISI) Web of Science (Thomson Reuters, New York, NY, USA) database. The search was performed on 15 November 2016. We searched the following terms either singly or in combination (“Laparoscopy” liver) OR TITLE: (“Laparoscopic” liver) OR TITLE: (“minimally” liver) OR TOPIC: (“Laparoscopy” hcc) OR TOPIC: (“Laparoscopy” hepatocellular carcinoma) OR TOPIC: (“Laparoscopy” hepatectomy) OR TOPIC: (“Laparoscopy” left lateral) OR TOPIC: (“Laparoscopy” posterior segment); Timespan: All years. Indexes: SCI-EXPANDED, SSCI, A&HCI, CPCI-S, CPCI-SSH, ESCI.
Inclusion and exclusion criteria
All article types were potentially included (original articles, review articles, case reports and series, systematic reviews/meta-analyses, letters or commentaries). A LLR article was defined by the following inclusion criteria: (I) content about liver surgery; (II) proposing new technique; (III) comparative study; (IV) indications, classifications and guidelines articles. Exclusion criteria were: (I) study on staging by laparoscopy; (II) non-surgical resection study (i.e., ablation or radiofrequency); (III) robotic surgery.
We found 2,018 papers, applying the exclusion criteria on all articles, the 100 most cited articles on LLR were identified (Figure 1). The top 100 articles and their associated number of citations are shown in Table 1. The number of top 100 articles citations ranged from 34 to 364 with a median of 70 (IQR 49–120) citations.
The oldest article was published in 1996 (ranked 12, 13, 56, 77, 88 and 91th) and the most recent in 2015 (45th). Sixty-one articles were published before the first consensus conference held in Louisville in 2008 (published in 2009). Eighty articles were published between 1990 and 2009. The 100 articles were published in 23 different journals (Table 2), 55 articles were published in 3 journals: Surgical Endoscopy , Annals of Surgery  and British Journal of Surgery .
The most frequent first and last authors were Dagher I (5 articles) and Cherqui D (7 articles) respectively. This result is reflected on the origin of the 100 articles: in 30 cases the article was published by a French team and in 18 cases by a USA team. This means that these two countries have contributed to half of the 100 most important articles on LLR. These results are resumed in Table 3. The topics of the articles were very heterogeneous in 46 cases (e.g., review, feasibility, consensus, personal experience). Nevertheless, if we look at the remaining 54 articles the main topic was: hepatocellular carcinoma in 17 cases, liver cysts of any kind in 9, major hepatectomies in 8, left lateral resections in 7, colorectal metastases in 6, Bening diseases in 4 and in living donor hepatectomies in 3.
Analyzing the 1,086 articles included in this study, the number of publication grew constantly, with more than 100 publications per year since 2014. The number of citations increased accordingly and it is now of over 2,000 per year (Figures 2,3).
Laparoscopic liver surgery is out of doubt one of the fastest growing fields in abdominal surgery today. The technical evolution led to the expansion of the indications without jeopardizing the outcomes. The world review of LLR published in 2009 reported a global experience of 2,804 cases (3). That review is actually the most cited article on LLR. The second most cited article is the first International Position on Laparoscopic Liver Surgery (2).
After the release of the Louisville Statement and the first world review, there has been a substantial increase in the number of published articles and citations per year (namely, >80 articles and >1,000 citations) (Figures 2,3). Despite this growing interest in the field, we found a mean of only 70 citations per article for the top 100 articles. This is probably due to LLR still being a very specialized topic in hepatic surgery with a limited number of authors publishing about it. Also, most of the authors of the 100 top articles are either from France or USA (Table 3), highlighting again that LLR is performed, especially at high volumes, only in a few centers. Nevertheless, all continents are represented with at least one country in the top 100 articles as to show that LLR is spreading around the world.
According to the International Position on LLR, many centers have shown a steady increase in the number of resections each year and publications seem to have followed as a consequence. In the same paper, a consensus of experts proposed the best indications for LLR: a solitary lesion less than 5 cm in diameter and nodules located in the anterior segments (2,4). Technical recommendations included that LLR should be applied far from the hepatic hilum, and the vena cava. Concerning the oncological proficiency with LLR, this should only be adopted if adequate margins can be obtained laparoscopically, keeping a safety distance of the nodule from the line of transection. Six years after the Louisville statement, the Second International Consensus Conference on LLR was held in Morioka, Japan, in 2014 to evaluate the current status of laparoscopic liver surgery and to provide strong recommendations to aid its future development (4). These two consensus conferences have outlined that the indications for LLR are continually expanding. The laparoscopic left lateral sectionectomy is defined as a gold standard procedure (5). Moreover, laparoscopic major hepatectomies are more often proposed as an evolution in the standard of care (6). Even malignancies such as colorectal metastases (7) or HCC (8,9) have been included as standard of care in selected cases. HCC as an indication for LLR is probably the most interesting one and with the greatest potentiality (10). This could explain why seventeen of the top 100 articles on LLR are focused on resections for HCC. LLR for HCC has been shown to improve postoperative morbidity even in patients with Child B cirrhosis (11). Nevertheless, in case of salvage liver transplantation after a laparoscopic resection for HCC, outcomes are comparable to patients who had open surgery including operative time, oncologic radicality, morbidity and mortality, but with the added advantages of laparoscopic surgery such as earlier return to mobility, lower blood losses and less pain (12,13).
Laparoscopic living donor hepatectomy for liver transplantation may encourage both donors and recipients to opt for this type of practice thanks to the reduced invasiveness and higher appeal associated with LLR. However, this procedure is a recognized technical challenge for the surgeon who is probably why we could find only three articles within the top 100 articles on LLR.
Minimally invasive approaches are expected to continue to gain space in liver surgery in the near future. One of the next goals for LLR will be to standardize the practice of resections for HCC in patients with cirrhosis. Surgery for living liver donation remains an extremely challenging field for pure laparoscopic surgery and the aid of robotic assistance could help popularize the adoption of minimally invasive approaches (14).
Having analyzed the 100 top articles on LLR, two main points are to be emphasized: LLR is now performed worldwide and surgical indications are continuing to expand. Furthermore, published articles on LLR are growing proportionally to its widespread. Randomized and prospective studies will be needed to build evidence around this topic and to strengthen the recommendations which to date are mainly based on promising clinical series only.
Conflicts of Interest: The authors have no conflicts of interest to declare.
- Gagner M, Rheault M, Dubuc J. Laparoscopic partial hepatectomy for liver tumor. Surg Endosc 1992;6:99.
- Buell JF, Cherqui D, Geller DA, et al. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009;250:825-30. [Crossref] [PubMed]
- Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg 2009;250:831-41. [Crossref] [PubMed]
- Wakabayashi G, Cherqui D, Geller DA, et al. Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 2015;261:619-29. [PubMed]
- Chang S, Laurent A, Tayar C, et al. Laparoscopy as a routine approach for left lateral sectionectomy. Br J Surg 2007;94:58-63. [Crossref] [PubMed]
- Dagher I, O'Rourke N, Geller DA, et al. Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg 2009;250:856-60. [Crossref] [PubMed]
- Fuks D, Nomi T, Ogiso S, et al. Laparoscopic two-stage hepatectomy for bilobar colorectal liver metastases. Br J Surg 2015;102:1684-90. [Crossref] [PubMed]
- Goumard C, Komatsu S, Brustia R, et al. Technical feasibility and safety of laparoscopic right hepatectomy for hepatocellular carcinoma following sequential TACE-PVE: a comparative study. Surg Endosc 2017;31:2340-9. [Crossref] [PubMed]
- Levi Sandri GB, Colasanti M, Santoro R, et al. Laparoscopic right hepatectomy for hepatocellular carcinoma in cirrhotic patient. Hepatobiliary Surg Nutr 2015;4:436-8. [PubMed]
- Levi Sandri GB, de Werra E, Mascianà G, et al. Laparoscopic and robotic approach for hepatocellular carcinoma-state of the art. Hepatobiliary Surg Nutr 2016;5:478-84. [Crossref] [PubMed]
- Ettorre GM, Levi Sandri GB. Laparoscopic approach for hepatocellular carcinoma: where is the limit? Chin J Cancer Res 2014;26:222-3. [PubMed]
- Laurent A, Tayar C, Andréoletti M, et al. Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2009;16:310-4. [Crossref] [PubMed]
- Felli E, Cillo U, Pinna AD, et al. Salvage liver transplantation after laparoscopic resection for hepatocellular carcinoma: a multicenter experience. Updates Surg 2015;67:215-22. [Crossref] [PubMed]
- Levi Sandri GB, de Werra E, Mascianà G, et al. The use of robotic surgery in abdominal organ transplantation: A literature review. Clin Transplant 2017.31. [PubMed]
Cite this article as: Levi Sandri GB, Spoletini G. The one hundred most-cited articles on laparoscopic liver surgery. Laparosc Surg 2017;1:3.