- Primary research
- Open Access
Laparoscopic spleen-preserving hilar lymph node dissection through pre-pancreatic and retro-pancreatic approach in patients with gastric cancer
- Liansheng Zheng†1, 2,
- Ce Zhang†1,
- Da Wang1, 3,
- Qi Xue1,
- Xiaoping Liu1,
- Ke-Jian Zhou1,
- Hao Liu1Email author and
- Guoxin Li1Email author
© The Author(s) 2016
- Received: 5 November 2015
- Accepted: 4 May 2016
- Published: 29 June 2016
The conventional radical resection of proximal gastric cancer is even more risky when performed laparoscopically, though this technique is widely used in gastrointestinal surgery and is accepted as the superior method. This paper explores the feasibility of laparoscopic spleen-preserving hilar lymph node dissection using a retro-pancreatic approach for the treatment of proximal gastric cancer.
Two cadavers were dissected for examination of and the pre-pancreatic and retro-pancreatic spaces. Following the dissection of the cadavers, ten live patients with proximal gastric cancer from May 2008 to May 2013 at Nanfang Hospital, Guangzhou, China, were given total gastrectomy and adjuvant splenic hilar lymph node clearance through pre-pancreatic and retro-pancreatic approach on the precondition of preserving the pancreas and spleen. The clinicopathologic characteristics, as well as the intraoperative and postoperative variables affecting the procedure, were observed and analyzed.
Anatomy of the space anterior and posterior to the pancreas in the two cadavers demonstrated the feasibility of pre-pancreatic and retro-pancreatic approach. The surgeries were all successfully performed laparoscopically; conversion to laparotomy was not necessary for any of the ten patients. The overall mean operative time was 243.6 ± 45 min. The mean estimated blood loss was 232 ± 80 ml. At the time of follow-up (median 12 months post-surgery), there had been neither local recurrence nor mortality in any of the patients.
Laparoscopic spleen- and pancreas-preserving splenic hilar lymph node dissection during total gastrectomy, using both pre-pancreatic and retro-pancreatic approaches, is indicated as a safe and feasible method for the treatment of proximal gastric cancer.
- Gastric cancer
- Splenic hilum
- Lymph node dissection
Gastric cancer is the second most common cause of all cancer-related deaths worldwide [1, 2]. Proximal gastric cancer has a higher annual incident rate than all other types of gastric carcinoma . Gastric cancer is not usually detected until it has reached an advanced stage. Total gastrectomy with D2 lymph node dissection is a standard course of treatment for individuals with advanced proximal cancer. In accordance with the Japanese Gastric Cancer Treatment Guidelines , splenic hilar lymph nodes are considered part of station 2 for radical resection of advanced proximal gastric cancer, which validates the need to dissect lymph nodes at the splenic hilum .
The conventional radical resection of proximal gastric cancer generally includes dissection of the stomach, the pancreatic tail, and the spleen . It may also consist of resection of the stomach and spleen, but the pancreas will be preserved [7, 8]. However, this method not only fails to improve the survival rate of patients, but it also increases instances of postoperative complications and mortality. For example, this conventional method results in higher incidences of pancreatic fistula, acute pancreatitis, abdominal abscess, postoperative diabetes, and postoperative hemorrhage [9–13]. The conventional radical resection of proximal gastric cancer is even more risky when performed laparoscopically, though this technique is widely used in gastrointestinal surgery and is accepted as the superior method. Based on this information, we evaluated the anatomy of the cadavers and used laparoscopic techniques on the live patients to identify an optimal surgical method for preserving the functions of the pancreas and spleen while reducing postoperative complications and mortality rates.
Two cadavers, a female and a male, were provided by Southern Medical University in Guangzhou, China, for use in the study. The cadavers were preserved at −20 °C. Next, they were defrosted and dissected at 4 °C. A digital camera (EOS 20D Canon, Tokyo, Japan) was used to record the observations.
Patient characteristics and surgical outcomes
The total number of patients
3 (30 %)
7 (70 %)
7 (70 %)
3 (30 %)
The depth of tumor invasion
4 (40 %)
6 (60 %)
1 (10 %)
3 (30 %)
4 (40 %)
2 (20 %)
The average hospitalization days
11.5 ± 3
Mean operating time
243.6 ± 45
Mean bleeding volume
232 ± 80
1 (10 %)
7 (70 %)
2 (20 %)
A surgical group with experience in laparoscopic gastric cancer surgery performed the surgeries. After general anesthesia, the patient was placed in the reverse Trendelenburg position. The surgeon stood at the patient’s left side, with the first assistant at the patient’s right and the camera operator between the patient’s legs. Five holes were made in the abdominal wall, and CO2 pressure was maintained at 12–14 mmHg. Surgery proceeded using the pre-pancreatic and retro-pancreatic approach.
The results of cadaver dissection
Consequently, from the perspective of cadaveric anatomy, the lymph nodes peripheral to the pancreatic artery and those located at the splenic hilum superior to the pancreatic tail could be cleaned along the splenic artery in the pre-pancreatic space, while the lymph nodes peripheral to the pancreatic vein and those located at the splenic hilum inferior to the pancreatic tail might be swept away along the splenic vein in the retro-pancreatic space.
The surgical procedures of live patients
Clinicopathological parameters for the patients
Seven males and three females, with an average age of 58.3 ± 17.6 years (39–76 years old), were included in this study. The mean operation time was 243.6 ± 45 min (Table 1). The hemorrhage volume was 232 ± 80 ml (Table 1). The length of hospital stay was approximately 11.5 ± 3 days (Table 1). Generally, the operations proceeded without complications, with only one patient suffering a 1 cm laceration and hemorrhage in the splenic capsule during the dissection of the splenic hilar lymph nodes. This hemorrhage was stopped using electrocautery and gauze. At the time of follow-up (median of 12 months), it was found that none of the patients had died or experienced recurrent or metastatic disease.
Pancreato splenectomy traditionally required the complete removal of LNs in the splenic hilar area to provide a normative D2 LN dissection. However, this method not only failed to improve survival rates among patients [7, 13, 15–17] but also increased mortality rates and postoperative complications. These complications included distinctly higher incidences of pancreatic fistula, acute pancreatitis, abdominal abscess, postoperative diabetes, and postoperative hemorrhages. To prevent some of these complications, surgeons began to adjust dissection procedures and focus on pancreas-preserving dissection of the total stomach and spleen . However, recent reports suggest that spleen dissection may not improve patient survival rates [19, 20]; on the contrary, total spleen dissection may actually cause complications, such as compromising the immune system, spleen heat, blood loss, and portal thrombosis. Therefore, the standardized recommended procedures for open surgery to treat gastric cancer are as follows: subsequent dissection of the gastrocolic ligament, the splenocolic ligament, and the splenorenal ligament and dissociation of the anterior lobe of the mesocolon to the inferior margin of the pancreas. These standardizations also include skeletonization of the splenic artery and vein; adjustment of the pancreatic body, the pancreatic tail, and the spleen through the incision via the retro-pancreatic space; and removal of the splenic hilar lymph nodes using pre-pancreatic and retro-pancreatic approaches that aim to preserve the pancreas and spleen.
Advances in laparoscopic techniques have led to a decrease in the use of open surgery. Laparoscopy initially focused exclusively on abdominal detection, but it was then expanded to include cholecystectomy and colorectal resection, after which it was utilized for conventional resection of the stomach, spleen, and pancreas. Based on these developments, this paper proposes that laparoscopic technology can achieve effects equal to those achieved with the aforementioned open surgery to treat gastric cancer. Because laparoscopic surgeries do not allow for the spleen, pancreatic body, and tail to be removed through the incision, some doubts persist regarding the removal of splenic hilar lymph nodes using pre-pancreatic and retro-pancreatic approaches. Nevertheless, the cadaveric anatomy presented in this paper indicates the existence of a relatively large space anterior to the pancreas, which is ideal for laparoscopic surgery, as well as a similarly convenient normal inter-fascia space free of vessels and nerves. Based on the cadaveric anatomy observed in this study, the researchers who conducted this study successfully conducted ten dissections of splenic hilar lymph nodes using pre-pancreatic and retro-pancreatic approaches, and in doing so, we were able to preserve the pancreases and spleens of all ten patients.
Some surgeons advise en bloc resection of gastric tumors, peripheral lymphatic tissues, and splenic hilar lymphatic tissues. However, this technique makes surgery more difficult. When removing the lymph nodes peripheral to the splenic vein by flipping the pancreatic body and tail, improper traction and exposure are likely to cause lacerations of the splenic vein, creating massive hemorrhages. Therefore, this study suggests that tumors and peripheral lymphatic tissues be removed prior to the dissection of splenic hilar lymphatic tissues. This suggested procedural change not only broadens the space for operations and reduces technical difficulties but also facilitates the management of emergencies (such as laceration of the splenic vein).
This procedure is ideal for patients without distal metastasis or obvious fibrosis of enlarged splenic hilar lymph nodes. If the preoperative examination identifies direct extension of the tumor to the spleen and distal pancreas, or if it shows definite LN metastasis at the splenic hilum, then dissection of the entire stomach and spleen is preferable. This is primarily due to the high incidence of postoperative complications and increased mortality rates.
There were some limitations to this study. The sample size was small, no control group was used, and long-term follow-ups were not conducted. However, the preliminary findings from this study demonstrate that for the treatment of proximal gastric cancer, laparoscopic spleen-preserving dissection of the hilar lymph nodes using pre-pancreatic and retro-pancreatic approaches is technically feasible. The study also indicates that this procedure is easy to master and could easily be adopted on a wide scale. However, multicenter, randomized controlled trials that evaluate the long-term outcome of this procedure are necessary to establish the technique’s effectiveness as a cure for proximal gastric cancer.
LZ, CZ writing of the manuscript; LZ, DW, CZ: anatomic observation and data collection; LZ, DW: statistical analysis; LZ, GL: design and supervision of the study. All authors read and approved the final manuscript.
This study is supported by the Key Clinical Specialty Discipline Construction Program, the Research Fund of Public welfare in Health Industry (No. 201402015), the Major Program of Science and Technology Program of Guangzhou (No. 201300000087), and the National Key Technology R&D Program (No. 2013BAI05B00).
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol Off J Am Soc Clin Oncol. 2006;24(14):2137–50.View ArticleGoogle Scholar
- Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: gLOBOCAN 2008. Int J Cancer J Int du Cancer. 2010;127(12):2893–917.View ArticleGoogle Scholar
- Huang CM, Wang JB, Lu HS, Zheng CH, Li P, Xie JW, Zhang XF. Prognostic impact of splenectomy on advanced proximal gastric cancer with No. 10 lymph node metastasis. Chin Med J. 2009;122(22):2757–62.PubMedGoogle Scholar
- Japanese Gastric Cancer A. Japanese classification of gastric carcinoma—2nd english edition. Gastric Cancer Off J Int Gastric Cancer Assoc Japanese Gastric Cancer Assoc. 1998;1(1):10–24.Google Scholar
- Japanese Gastric Cancer A. Japanese gastric cancer treatment guidelines 2010 (version 3). Gastric Cancer Off J Int Gastric Cancer Assoc Japanese Gastric Cancer Assoc. 2011;14(2):113–23.Google Scholar
- Brunschwig A. Pancreato-total gastrectomy and splenectomy for advanced carcinoma of the stomach. Cancer. 1948;1(3):427–30.View ArticlePubMedGoogle Scholar
- Csendes A, Burdiles P, Rojas J, Braghetto I, Diaz JC, Maluenda F. A prospective randomized study comparing D2 total gastrectomy versus D2 total gastrectomy plus splenectomy in 187 patients with gastric carcinoma. Surgery. 2002;131(4):401–7.View ArticlePubMedGoogle Scholar
- Sakaguchi T, Sawada H, Yamada Y, Fujimoto H, Emoto K, Takayama T, Ueno M, Nakajima Y. Indication of splenectomy for gastric carcinoma involving the proximal part of the stomach. Hepato-gastroenterology. 2001;48(38):603–5.PubMedGoogle Scholar
- Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P. Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. Surgical Co-operative Group. Br J Cancer. 1999;79(9–10):1522–30.View ArticlePubMedPubMed CentralGoogle Scholar
- Yu W, Choi GS, Chung HY. Randomized clinical trial of splenectomy versus splenic preservation in patients with proximal gastric cancer. Br J Surg. 2006;93(5):559–63.View ArticlePubMedGoogle Scholar
- Weitz J, Jaques DP, Brennan M, Karpeh M. Association of splenectomy with postoperative complications in patients with proximal gastric and gastroesophageal junction cancer. Ann Surg Oncol. 2004;11(7):682–9.View ArticlePubMedGoogle Scholar
- Furukawa H, Hiratsuka M, Ishikawa O, Ikeda M, Imamura H, Masutani S, Tatsuta M, Satomi T. Total gastrectomy with dissection of lymph nodes along the splenic artery: a pancreas-preserving method. Ann Surg Oncol. 2000;7(9):669–73.View ArticlePubMedGoogle Scholar
- Okinaga K, Iinuma H, Kitamura Y, Yokohata T, Inaba T, Fukushima R. Effect of immunotherapy and spleen preservation on immunological function in patients with gastric cancer. J Exp Clin Cancer Res CR. 2006;25(3):339–49.PubMedGoogle Scholar
- Zhang C, Yu J, Wang YN, Hu YF, Li GX. Living anatomical observations on peripancreatic spaces and their implications on laparoscopic gastrectomy with D(2) lymphadenectomy for distal gastric cancer. Zhonghua wei chang wai ke za zhi Chin J Gastrointest Surg. 2009;12(2):117–20.Google Scholar
- Schwarz RE. Spleen-preserving splenic hilar lymphadenectomy at the time of gastrectomy for cancer: technical feasibility and early results. J Surg Oncol. 2002;79(1):73–6.View ArticlePubMedGoogle Scholar
- Fatouros M, Roukos DH, Lorenz M, Arampatzis I, Hottentrott C, Encke A, Kappas AM. Impact of spleen preservation in patients with gastric cancer. Anticancer Res. 2005;25(4):3023–30.PubMedGoogle Scholar
- Degiuli M, Sasako M, Ponzetto A, Allone T, Soldati T, Calgaro M, Balcet F, Bussone R, Olivieri F, Scaglione D, Danese F, Morino M, Calderini P, Capussotti L, Fronda G, Garavoglia M, Locatelli L, Dellepiane M, Rossini FP, Calvo F. Extended lymph node dissection for gastric cancer: results of a prospective, multi-centre analysis of morbidity and mortality in 118 consecutive cases. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol. 1997;23(4):310–4.Google Scholar
- Toge T, Kameda A, Kuroi K, Seto Y, Yamada H, Hattori T. The role of the spleen in immunosuppression and the effects of splenectomy on prognosis in gastric cancer patients. Nihon Geka Gakkai zasshi. 1985;86(9):1120–3.PubMedGoogle Scholar
- Zhang CH, Zhan WH, He YL, Chen CQ, Huang MJ, Cai SR. Spleen preservation in radical surgery for gastric cardia cancer. Ann Surg Oncol. 2007;14(4):1312–9.View ArticlePubMedGoogle Scholar
- Shin SH, Jung H, Choi SH, An JY, Choi MG, Noh JH, Sohn TS, Bae JM, Kim S. Clinical significance of splenic hilar lymph node metastasis in proximal gastric cancer. Ann Surg Oncol. 2009;16(5):1304–9.View ArticlePubMedGoogle Scholar