Technical pro & cons of the laparoscopic lymphadenectomy
Review Article

Technical pro & cons of the laparoscopic lymphadenectomy

Riccardo Rosati, Paolo Parise, Fabio Giannone Codiglione

Gastroenterological Surgery Unit, San Raffaele Hospital, Vita-Salute University, Via Olgettina 60, 20132, Milan, Italy

Contributions: (I) Conception and design: R Rosati, P Parise; (II) Administrative support: P Parise, F Giannone Codiglione; (III) Provision of study materials or patients: P Parise, F Giannone Codiglione; (IV) Collection and assembly of data: F Giannone Codiglione; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Dott. Paolo Parise. Gastroenterological Surgery Unit, San Raffaele Hospital, Via Olgettina, 60, 20132, Milan, Italy. Email:

Abstract: Laparoscopy has been introduced in treatment of gastric cancer to reduce surgical trauma and to improve post-operative functional recovery. Most of international guidelines allow the use of this minimally invasive approach in general surgical practice only in clinical stage I. One of the most important concerns in fact is the feasibility of D2 lymphadenectomy through laparoscopy. Reduced numbers of harvested lymph nodes have been reported, particularly in stations with a more difficult access. Nevertheless subsequent papers reported adequate numbers of total number of nodes retrieved, even with D2 dissection and even in complex stations but results from randomized controlled trials still lack. Laparoscopic approach has been proven safe and effective also in extremely complex maneuvers as spleen-preserving retropancreatic lymphadenectomy. The minimally invasive approach in D2 lymphadenectomy seems to be associated to comparable incidence of specific complications as compared to open surgery. The use of laparoscopy has extended the operating time but has reduced the blood loss. Because of high complexity of this kind surgery, laparoscopic gastric surgery for cancer should be done only in referral centers.

Keywords: Gastric neoplasms; lymph node excision; laparoscopy

Received: 02 September 2016; Accepted: 24 November 2016; Published: 27 December 2016.

doi: 10.21037/tgh.2016.12.04


As in other fields of surgery, laparoscopy has been introduced in oncologic gastric surgery aiming to reduce the surgical trauma and allow a faster recovery of patients. In 1994 Kitano (1) first reported a laparoscopic gastric resection for early gastric cancer (EGC) and in 2001 Goh et al. (2) first published a laparoscopic assisted gastrectomy with a D2 lymphadenectomy for advanced gastric cancer (AGC).

Nowadays guidelines of the Japanese Gastric Cancer Association consider the laparoscopic approach an adequate treatment in general clinical practice only in stage I cancer in which a distal gastrectomy is indicated. Cases of AGC or those in whom a total gastrectomy is indicated, should be treated by a laparoscopic approach only in clinical trials and at high volume centers (3). Similar positions have been taken also in the West by the European Society of Medical Oncology, European Society of Surgical Oncology and European Society of Radiotherapy and Oncology and in Italy by the Italian Research Group for Gastric Cancer (4,5).

Materials and methods

A Medline search for gastric neoplasms, lymph node excision, lymphadenectomy and laparoscopy was made. Case reports and small case-series were excluded.

Feasibility of an adequate D2 lymphadenectomy

One of the reasons for this limited area of application of laparoscopy is the concern about the feasibility of an adequate D2 lymphadenectomy. In fact by a technical point of view this is a very difficult and challenging procedure even in experienced hands. For example Miura reported a statistically significant lower number of harvested lymph nodes after laparoscopic gastric resection than open approach. In particular, the stations mainly involved were the No. 4, 6, 9 and 11 (6). Subsequently, other studies evidenced how the total number of harvested lymph nodes after laparoscopic or open gastric resection was similar (7,8). Nevertheless the total number of harvested lymph nodes is a fast but suboptimal index of the extension and effectiveness of a lymphadenectomy, because the minimum number of 15 nodes could be obtained even in presence of incomplete nodal dissections in the more difficult stations. Interestingly other authors reported even better performances with laparoscopic approach: Huang et al. in a paper comparing 506 laparoscopic gastric resection with 428 open retrieved significantly more lymph nodes with the mini-invasive technique at the station No. 7 and 8 (9). The finding of a higher number of nodes retrieved with the laparoscopic approach has been described also in other fields of surgery as colorectal and esophageal. Many explanations are possible: the first is that even if laparoscopic nodal dissection is difficult, with time and practice the surgeon becomes more skilled day by day overcoming the initial difficulties and capitalizing the better view and precision offered by laparoscopy. Modern laparoscopic cameras amplify nervous, vascular and fascial structures helping the surgeon to identify correct planes and dissecting lymph nodes. Moreover the last generation surgical instruments for tissue sealing and cutting allow the surgeon to gain an optimal hemostasis, reducing damages to surrounding structures and making lymphadenectomy easier and more extensive, with lesser risk of lymphatic leak from properly sealed lymphatic vessels.

Some authors speculated that a possible bias affecting the good results of laparoscopic D2 lymphadenectomy could be a lower BMI in minimally invasive treatment patients, but Lu et al. in a recent meta-analysis on ten non-randomized trials on distal gastrectomy evidenced how no statistically significant differences were found in terms of BMI and number of total lymph nodes harvested and rate of positive nodes between the two groups (10).

Spleen preserving lymphadenectomy

A particularly challenging maneuver by laparoscopy, when needed, is the spleen preserving lymphadenectomy of the stations No. 10. The first report of this maneuver was made by Hyung et al. in 2008 (11). This is an extremely difficult dissection because of the deep location of the splenic hilum, the narrow space and anatomical variability of the splenic artery branches. The risk of not easily manageable bleeding, of injuries to pancreas or spleen or adrenal gland is high and probably this is the reason why this procedure is not so diffuse, especially in Western countries. In fact a learning curve of about 40 cases has been proposed for this specific maneuver (12). Nevertheless it is technically feasible by laparoscopy and it is becoming more accepted by an increasing number of experts. Basically two approach are used: the first dissecting initially the stations No. 11p, 11d and then No. 10, the second dissecting station No. 10 first and subsequently the 11d and 11p (12). In order to preoperatively quantify the difficulty of this dissection Li et al. produced a “difficulty score” based on male gender, BMI >25, presence of splenic lobar arteries ≥3 and with a distributed-type and divided patients in three category of difficulty: low, intermediate and high. They found that most of patients were in the intermediate group (71.6%) but only 43.6% of them had a long lasting operation time. Only 13.9% of patients were in high difficulty group but 90.9% of them required a long operating time. They concluded that less skilled surgeons should face only low difficulty spleen preserving lymphadenectomy (13).

General considerations

The minimally invasive approach to D2 lymphadenectomy seems to be associated to a comparable incidence of specific complications as chyle leak, pancreatitis and pancreatic fistula as evidenced in a case-control study on 266 gastric cancer patients submitted to laparoscopic or open distal gastrectomy + D2 lymphadenectomy (14) and some recent meta-analysis on AGC and total gastrectomy in more than 2,000 patients (15,16).

Almost all reports from literature evidence how the laparoscopic approach to gastric cancer is associated with a longer operative time of about 60–90 minutes respect traditional open surgery and often is a statistically significant difference (14,16,17). Probably one of the main reasons is that the laparoscopic lymphadenectomy is a complex and time-consuming procedure, even if some authors now reports comparable operating time, suggesting that with practice our performances can be improved (18).

On the other hand, laparoscopy allows to halve the intraoperative blood loss and to reduce the need for blood transfusions as observed by many authors (17,18).


The laparoscopic D2 lymphadenectomy represents a challenging procedure for surgeons and dissection of some stations represents a really difficult step. Nevertheless available data, even if not always with high level of evidence, suggest that is a feasible procedure at least as effective as with open approach. A learning curve of 40 cases is suggested by many authors (19,20) but it’s an hard goal to reach, particularly for surgeons from countries where gastric cancer has not an high incidence. Even for this reason laparoscopic surgery for gastric cancer should be centralized in high volume centers in order to maximize results.




Conflicts of Interest: The authors have no conflicts of interest to declare.


  1. Kitano S, Iso Y, Moriyama M, et al. Laparoscopy-assisted Billroth I gastrectomy. Surg Laparosc Endosc 1994;4:146-8. [PubMed]
  2. Goh PM, Khan AZ, So JB, et al. Early experience with laparoscopic radical gastrectomy for advanced gastric cancer. Surg Laparosc Endosc Percutan Tech 2001;11:83-7. [Crossref] [PubMed]
  3. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2014 (ver. 4). Gastric Cancer 2016. [Epub ahead of print].
  4. Waddell T, Verheij M, Allum W, et al. Gastric cancer: ESMO-ESSO-ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2013;24 Suppl 6:vi57-63. [Crossref] [PubMed]
  5. De Manzoni G, Marrelli D, Baiocchi GL, et al. The Italian Research Group for Gastric Cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer 2016. [Epub ahead of print]. [Crossref] [PubMed]
  6. Miura S, Kodera Y, Fujiwara M, et al. Laparoscopy-assisted distal gastrectomy with systemic lymph node dissection: a critical reappraisal from the viewpoint of lymph node retrieval. J Am Coll Surg 2004;198:933-8. [Crossref] [PubMed]
  7. Huscher C, Mingoli A, Sgarzini G, et al. Value of extended lymphadenectomy in laparoscopic subtotal gastrectomy for advanced gastric cancer. J Am Coll Surg 2005;200:314. [Crossref] [PubMed]
  8. Song KY, Kim SN, Park CH. Laparoscopy-assisted distal gastrectomy with D2 lymph node dissection for gastric cancer: technical and oncologic aspects. Surg Endosc 2008;22:655-9. [Crossref] [PubMed]
  9. Huang CM, Lin JX, Zheng CH, et al. Effect of laparoscopy assisted vs. open radical gastrectomy on lymph node dissection in patients with gastric cancer. Zhonghua Wai Ke Za Zhi 2011;49:200-3. [PubMed]
  10. Lu C, Zhou S, Peng Z, et al. Quality of D2 lymphadenectomy for advanced gastric cancer: is laparoscopic-assisted distal gastrectomy as effective as open distal gastrectomy? Surg Endosc 2015;29:1537-44. [Crossref] [PubMed]
  11. Hyung WJ, Lim JS, Song J, et al. Laparoscopic spleen-preserving splenic hilar lymph node dissection during total gastrectomy for gastric cancer. J Am Coll Surg 2008;207:e6-11. [Crossref] [PubMed]
  12. Chen QY, Huang CM, Zheng CH, et al. Strategies of laparoscopic spleen-preserving splenic hilar lymph node dissection for advanced proximal gastric cancer. World J Gastrointest Surg 2016;8:402-6. [Crossref] [PubMed]
  13. Li P, Huang CM, Lin JX, et al. A preoperatively predictive difficulty scoring system for laparoscopic spleen-preserving splenic hilar lymph node dissection for gastric cancer: experience from a large-scale single center. Surg Endosc 2016;30:4092-101. [Crossref] [PubMed]
  14. Zhao XF, Jeong O, Jung MR, et al. A propensity score-matched case-control comparative study of laparoscopic and open extended (D2) lymph node dissection for distal gastric carcinoma. Surg Endosc 2013;27:2792-800. [Crossref] [PubMed]
  15. Wang W, Zhang X, Shen C, et al. Laparoscopic versus open total gastrectomy for gastric cancer: an updated meta-analysis. PLoS One 2014;9:e88753. [Crossref] [PubMed]
  16. Zou ZH, Zhao LY, Mou TY, et al. Laparoscopic vs open D2 gastrectomy for locally advanced gastric cancer: a meta-analysis. World J Gastroenterol 2014;20:16750-64. [Crossref] [PubMed]
  17. Sato H, Shimada M, Kurita N, et al. Comparison of long-term prognosis of laparoscopy-assisted gastrectomy and conventional open gastrectomy with special reference to D2 lymph node dissection. Surg Endosc 2012;26:2240-6. [Crossref] [PubMed]
  18. Lin JX, Huang CM, Zheng CH, et al. Laparoscopy-assisted gastrectomy with D2 lymph node dissection for advanced gastric cancer without serosa invasion: a matched cohort study from South China. World J Surg Oncol 2013;11:4. [Crossref] [PubMed]
  19. Zhou D, Quan Z, Wang J, et al. Laparoscopic-assisted versus open distal gastrectomy with D2 lymph node resection for advanced gastric cancer: effect of learning curve on short-term outcomes. a meta-analysis. J Laparoendosc Adv Surg Tech A 2014;24:139-50. [Crossref] [PubMed]
  20. Antonakis PT, Ashrafian H, Isla AM. Laparoscopic gastric surgery for cancer: where do we stand? World J Gastroenterol 2014;20:14280-91. [Crossref] [PubMed]
doi: 10.21037/tgh.2016.12.04
Cite this article as: Rosati R, Parise P, Giannone Codiglione F. Technical pro & cons of the laparoscopic lymphadenectomy. Transl Gastroenterol Hepatol 2016;1:93.