Surgical approaches for minimally invasive distal pancreatectomy: A systematic review
Daisuke Ban
Department of Hepatobiliary and Pancreatic Surgery, National Cancer Center Hospital, Tokyo, Japan
Search for more papers by this authorGiovanni Maria Garbarino
Department of Medical Surgical Science and Translational Medicine, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorYoshiya Ishikawa
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorGoro Honda
Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University, Tokyo, Japan
Search for more papers by this authorJin-Young Jang
Department of Surgery, Seoul National University College of Medicine, Seoul, Korea
Search for more papers by this authorChang Moo Kang
Department of Surgery, Yonsei University College of Medicine, Seoul, Korea
Search for more papers by this authorAya Maekawa
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorYoshiki Murase
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorYuichi Nagakawa
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorHitoe Nishino
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorTakao Ohtsuka
First Department of Surgery, Kagoshima University School of Medicine, Kagoshima, Japan
Search for more papers by this authorAnusak Yiengpruksawan
Minimally Invasive Surgery Division, Department of Surgery, Faculty of Medicine, Siriraj Hospital, Mahidol University, Bangkok, Thailand
Search for more papers by this authorItaru Endo
Department of Gastroenterological Surgery, Yokohama City University Graduate School of Medicine, Yokohama, Japan
Search for more papers by this authorAkihiko Tsuchida
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorCorresponding Author
Masafumi Nakamura
Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
Correspondence
Masafumi Nakamura, Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Fukuoka 812-8582, Japan.
Email: [email protected]
Search for more papers by this authorStudy group of Precision Anatomy for Minimally Invasive Hepato-Biliary-Pancreatic surgery (PAM-HBP surgery)
Search for more papers by this authorDaisuke Ban
Department of Hepatobiliary and Pancreatic Surgery, National Cancer Center Hospital, Tokyo, Japan
Search for more papers by this authorGiovanni Maria Garbarino
Department of Medical Surgical Science and Translational Medicine, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorYoshiya Ishikawa
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorGoro Honda
Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical University, Tokyo, Japan
Search for more papers by this authorJin-Young Jang
Department of Surgery, Seoul National University College of Medicine, Seoul, Korea
Search for more papers by this authorChang Moo Kang
Department of Surgery, Yonsei University College of Medicine, Seoul, Korea
Search for more papers by this authorAya Maekawa
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorYoshiki Murase
Department of Hepatobiliary and Pancreatic Surgery, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Search for more papers by this authorYuichi Nagakawa
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorHitoe Nishino
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorTakao Ohtsuka
First Department of Surgery, Kagoshima University School of Medicine, Kagoshima, Japan
Search for more papers by this authorAnusak Yiengpruksawan
Minimally Invasive Surgery Division, Department of Surgery, Faculty of Medicine, Siriraj Hospital, Mahidol University, Bangkok, Thailand
Search for more papers by this authorItaru Endo
Department of Gastroenterological Surgery, Yokohama City University Graduate School of Medicine, Yokohama, Japan
Search for more papers by this authorAkihiko Tsuchida
Department of Gastrointestinal and Pediatric Surgery, Tokyo Medical University, Tokyo, Japan
Search for more papers by this authorCorresponding Author
Masafumi Nakamura
Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
Correspondence
Masafumi Nakamura, Department of Surgery and Oncology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Fukuoka 812-8582, Japan.
Email: [email protected]
Search for more papers by this authorStudy group of Precision Anatomy for Minimally Invasive Hepato-Biliary-Pancreatic surgery (PAM-HBP surgery)
Search for more papers by this authorCollaborators are presented in Appendix 1.
Abstract
Background
Minimally invasive distal pancreatectomy (MIDP) was initially performed for benign tumors, but recently its indications have steadily broadened to encompass other conditions including pancreatic malignancies. Thorough anatomical knowledge is mandatory for precise surgery in the era of minimally invasive surgery. However, expert consensus regarding anatomical landmarks to facilitate the safe performance of MIDP is still lacking.
Methods
A systematic literature search was performed using keywords to identify articles regarding the vascular anatomy and surgical approaches/techniques for MIDP.
Results
All of the systematic reviews revealed that MIDP was not associated with an increase in postoperative complications. Moreover, most showed that MIDP resulted in less blood loss than open surgery. Regarding surgical approaches for MIDP, a standardized stepwise procedure improved surgical outcomes, including blood loss, operative time, and major complications. There are two approaches to the splenic vessels, superior and inferior; however, no study has ever directly compared them with respect to clinical outcomes. The morphology of the splenic artery affects the difficulty of approaching the artery's root. To select an appropriate dissecting layer when performing posterior resection, thorough knowledge of the anatomy of the fascia, left renal vein/artery, and left adrenal gland is needed.
Conclusions
In MIDP, a standardized approach and precise knowledge of anatomy facilitates safe surgery and has the advantage of a shorter learning curve. Anatomical features and landmarks are particularly important in cases of radical MIDP and splenic vessel preserving MIDP.
CONFLICT OF INTEREST
None declared.
Supporting Information
| Filename | Description |
|---|---|
| jhbp902-sup-0001-TableS1.docxWord 2007 document , 11.2 KB | Table S1 |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Vollmer CM, Asbun HJ, Barkun J, Besselink MG, Boggi U, Conlon KC, et al. Proceedings of the first international state-of-the-art conference on minimally-invasive pancreatic resection (MIPR). HPB (Oxford). 2017; 19(3): 171–7.
- 2Bassi C, Andrianello S. Identifying key outcome metrics in pancreatic surgery, and how to optimally achieve them. HPB (Oxford). 2017; 19(3): 178–81.
- 3Asbun HJ, Moekotte AL, Vissers FL, Kunzler F, Cipriani F, Alseidi A, et al. The Miami International Evidence-based Guidelines on Minimally Invasive Pancreas Resection. Ann Surg. 2020; 271(1): 1–14.
- 4Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ. 2009; 339:b2535.
- 5 SIGN 50: A guideline developer's handbook. Scottish Intercollegiate Guidelines Network (SIGN). Available from https://www.sign.ac.uk/media/1050/sign50_2019.pdf
- 6Gavriilidis P, Roberts KJ, Sutcliffe RP. Comparison of robotic vs laparoscopic vs open distal pancreatectomy. A systematic review and network meta-analysis. HPB (Oxford). 2019; 21(10): 1268–76.
- 7Ricci C, Casadei R, Taffurelli G, Toscano F, Pacilio CA, Bogoni S, et al. Laparoscopic versus open distal pancreatectomy for ductal adenocarcinoma: a systematic review and meta-analysis. J Gastrointest Surg. 2015; 19(4): 770–81.
- 8Venkat 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: 1048–59.
- 9Yang DJ, Xiong JJ, Lu HM, Wei Y, Zhang L, Lu S, et al. The oncological safety in minimally invasive versus open distal pancreatectomy for pancreatic ductal adenocarcinoma: a systematic review and meta-analysis. Sci Rep. 2019; 9(1): 1159.
- 10Yi X, Chen S, Wang W, Zou L, Diao D, Zheng Y, et al. A systematic review and meta-analysis of laparoscopic and open distal pancreatectomy of nonductal adenocarcinomatous pancreatic tumor (NDACPT) in the pancreatic body and tail. Surg Laparosc Endosc Percutan Tech. 2017; 27(4): 206–19.
- 11Zhao W, Liu C, Li S, Geng D, Feng Y, Sun M. Safety and efficacy for robot-assisted versus open pancreaticoduodenectomy and distal pancreatectomy: a systematic review and meta-analysis. Surg Oncol. 2018; 27(3): 468–78.
- 12de Rooij T, van Hilst J, van Santvoort H, Boerma D, van den Boezem P, Daams F, et al. Minimally invasive versus open distal pancreatectomy (LEOPARD): a multicenter patient-blinded randomized controlled trial. Ann Surg. 2019; 269(1): 2–9.
- 13Bjornsson B, Larsson AL, Hjalmarsson C, Gasslander T, Sandstrom P. Comparison of the duration of hospital stay after laparoscopic or open distal pancreatectomy: randomized controlled trial. Br J Surg. 2020; 107: 1281–1288.
- 14van Hilst J, de Rooij T, Klompmaker S, Rawashdeh M, Aleotti F, Al-Sarireh B, et al. Minimally invasive versus open distal pancreatectomy for ductal adenocarcinoma (DIPLOMA): a pan-European propensity score matched study. Ann Surg. 2019; 269(1): 10–7.
- 15Asbun HJ, Stauffer JA. Laparoscopic approach to distal and subtotal pancreatectomy: a clockwise technique. Surg Endosc. 2011; 25(8): 2643–9.
- 16Asbun HJ, Van Hilst J, Tsamalaidze L, Kawaguchi Y, Sanford D, Pereira L, et al. Technique and audited outcomes of laparoscopic distal pancreatectomy combining the clockwise approach, progressive stepwise compression technique, and staple line reinforcement. Surg Endosc. 2020; 34(1): 231–9.
- 17Takaori K, Uemoto S. Artery-first distal pancreatectomy. Dig Surg. 2016; 33(4): 314–9.
- 18Inoko K, Ebihara Y, Sakamoto K, Miyamoto N, Kurashima Y, Tamoto E, et al. Strategic approach to the splenic artery in laparoscopic spleen-preserving distal pancreatectomy. Surg Laparosc Endosc Percutan Tech. 2015; 25(4): e122–5.
- 19Morikawa T, Ishida M, Takadate T, Hata T, Iseki M, Kawaguchi K, et al. The superior approach with the stomach roll-up technique improves intraoperative outcomes and facilitates learning laparoscopic distal pancreatectomy: a comparative study between the superior and inferior approach. Surg Today. 2020; 50(2): 153–62.
- 20Ishikawa Y, Ban D, Watanabe S, Akahoshi K, Ono H, Mitsunori Y, et al. Splenic artery as a simple landmark indicating difficulty during laparoscopic distal pancreatectomy. Asian J Endosc Surg. 2019; 12(1): 81–7.
- 21Kawasaki K, Kanaji S, Kobayashi I, Fujita T, Kominami H, Ueno K, et al. Multidetector computed tomography for preoperative identification of left gastric vein location in patients with gastric cancer. Gastric Cancer. 2010; 13(1): 25–9.
- 22Nagakawa Y, Sahara Y, Hosokawa Y, Takishita C, Kasuya K, Tsuchida A. The straightened splenic vessels method improves surgical outcomes of laparoscopic distal pancreatectomy. Dig Surg. 2017; 34(4): 289–97.
- 23Abu Hilal M, Richardson JR, de Rooij T, Dimovska E, Al-Saati H, Besselink MG. Laparoscopic radical 'no-touch' left pancreatosplenectomy for pancreatic ductal adenocarcinoma: technique and results. Surg Endosc. 2016; 30(9): 3830–8.
- 24Kim S, Yoon Y-S, Han H-S, Cho JY. Laparoscopic subtotal pancreatectomy with radical antegrade modular pancreatosplenectomy for left-sided pancreatic cancer. Surg Oncol. 2019; 28: 150.
- 25Lee SH, Kang CM, Hwang HK, Choi SH, Lee WJ, Chi HS. Minimally invasive RAMPS in well-selected left-sided pancreatic cancer within Yonsei criteria: long-term (>median 3 years) oncologic outcomes. Surg Endosc. 2014; 28(10): 2848–55.
- 26Yamamoto M, Zaima M, Yamamoto H, Harada H, Kawamura J, Yamada M, et al. New laparoscopic procedure for left-sided pancreatic cancer-artery-first approach laparoscopic RAMPS using 3D technique. World J Surg Oncol. 2017; 15(1): 213.
- 27Seyama Y, Doi M, Muto J. Laparoscopic distal pancreatectomy for left-sided pancreatic cancer using the “Caudo-Dorsal Artery First Approach”. Ann Surg Oncol. 2019; 26(13): 4464–5.
- 28Ome Y, Hashida K, Yokota M, Nagahisa Y, Michio O, Kawamoto K. Laparoscopic radical antegrade modular pancreatosplenectomy for left-sided pancreatic cancer using the ligament of Treitz approach. Surg Endosc. 2017; 31(11): 4836–7.
- 29Kitagawa H, Tajima H, Nakagawara H, Makino I, Miyashita T, Terakawa H, et al. A modification of radical antegrade modular pancreatosplenectomy for adenocarcinoma of the left pancreas: significance of en bloc resection including the anterior renal fascia. World J Surg. 2014; 38(9): 2448–54.
- 30Strasberg SM, Linehan DC, Hawkins WG. Radical antegrade modular pancreatosplenectomy procedure for adenocarcinoma of the body and tail of the pancreas: ability to obtain negative tangential margins. J Am Coll Surg. 2007; 204(2): 244–9.
- 31Nishino H, Nagakawa Y, Takishita C, Kozono S, Osakabe H, Nakagawa N, et al. Safe exposure of the left renal vein during laparoscopic distal pancreatectomy for pancreatic ductal adenocarcinoma: anatomical variations and pitfalls. Surg Today. 2020; 50(12): 1664–71.
- 32Cho A, Yamamoto H, Kainuma O, Ota T, Park S, Ikeda A, et al. Pure laparoscopic distal pancreatectomy with en bloc celiac axis resection. J Laparoendosc Adv Surg Tech A. 2011; 21(10): 957–9.
- 33Giulianotti PC, Addeo P, Buchs NC, Ayloo SM, Bianco FM. Robotic extended pancreatectomy with vascular resection for locally advanced pancreatic tumors. Pancreas. 2011; 40(8): 1264–70.
- 34Kimura W, Inoue T, Futakawa N, Shinkai H, Han I, Muto T. Spleen-preserving distal pancreatectomy with conservation of the splenic artery and vein. Surgery. 1996; 120(5): 885–90.
- 35Warshaw AL. Conservation of the spleen with distal pancreatectomy. Arch Surg. 1988; 123(5): 550–3.
- 36Warshaw AL. Distal pancreatectomy with preservation of the spleen. J Hepatobiliary Pancreat Sci. 2010; 17(6): 808–12.
- 37Macchi V, Picardi EEE, Porzionato A, Morra A, Bardini R, Loukas M, et al. Anatomo-radiological patterns of pancreatic vascularization, with surgical implications: Clinical and anatomical study. Clin Anat. 2017; 30(5): 614–24.
- 38Hongo N, Mori H, Matsumoto S, Okino Y, Ueda S, Shuto R. Anatomical variations of peripancreatic veins and their intrapancreatic tributaries: multidetector-row CT scanning. Abdom Imaging. 2010; 35(2): 143–53.
- 39Nakata K, Ohtsuka T, Mori Y, Miyasaka Y, Nakamura M. Laparoscopic spleen-preserving distal pancreatectomy. Tan to Sui. 2018; 39: 1239–45. [published in Japanese].
- 40Nakamura M, Nagayoshi Y, Kono H, Mori Y, Ohtsuka T, Takahata S, et al. Lateral approach for laparoscopic splenic vessel-preserving distal pancreatectomy. Surgery. 2011; 150(2): 326–31.
- 41Hua YF, Yadav DK, Bai X, Liang T. Laparoscopic spleen-preserving distal pancreatectomy (LSPDP) with preservation of splenic vessels: an inferior-posterior approach. Gastroenterol Res Pract. 2018; 2018:1683719.
- 42Misawa K. Spleen-preserving laparoscopic distal pancreatectomv: indication, procedure, and usefulness of Warshaw procedure. Tan to Sui. 2018; 39(11): 1247–53. [published in Japanese].
- 43Sato Y, Shimoda S, Takeda N, Tanaka N, Hatakeyama K. Evaluation of splenic circulation after spleen-preserving distal pancreatectomy by dividing the splenic artery and vein. Dig Surg. 2000; 17(5): 519–22.
- 44Egorov VI, Yashina NI, Zhurenkova TV, Petukhova MV, Starostina NS, Zarinskaya SA, et al. Spleen-preserving distal pancreatectomy with resection of the splenic vessels. Should one rely on the short gastric arteries? Jop. 2011; 12(5): 445–57.
- 45Romero-Torres R. The true splenic blood supply and its surgical applications. Hepatogastroenterology. 1998; 45(21): 885–8.
- 46Fernández-Cruz L, Martínez I, Gilabert R, Cesar-Borges G, Astudillo E, Navarro S. Laparoscopic distal pancreatectomy combined with preservation of the spleen for cystic neoplasms of the pancreas. J Gastrointest Surg. 2004; 8(4): 493–501.
- 47Rosado ID, Bhalla S, Sanchez LA, Fields RC, Hawkins WG, Strasberg SM. Pattern of venous collateral development after splenic vein occlusion in an extended Whipple procedure (Whipple at the splenic artery) and long-term results. J Gastrointest Surg. 2017; 21(3): 516–26.
- 48Ono Y, Matsueda K, Koga R, Takahashi Y, Arita J, Takahashi M, et al. Sinistral portal hypertension after pancreaticoduodenectomy with splenic vein ligation. Br J Surg. 2015; 102(3): 219–28.
- 49Ohtsuka T, Ban D, Nakamura Y, Nagakawa Y, Tanabe M, Gotoh Y, et al. Difficulty scoring system in laparoscopic distal pancreatectomy. J Hepatobiliary Pancreat Sci. 2018; 25(11): 489–97.
- 50Grossman JG, Fields RC, Hawkins WG, Strasberg SM. Single institution results of radical antegrade modular pancreatosplenectomy for adenocarcinoma of the body and tail of pancreas in 78 patients. J Hepatobiliary Pancreat Sci. 2016; 23(7): 432–41.
- 51Nakata K, Shikata S, Ohtsuka T, Ukai T, Miyasaka Y, Mori Y, et al. Minimally invasive preservation versus splenectomy during distal pancreatectomy: a systematic review and meta-analysis. J Hepatobiliary Pancreat Sci. 2018; 25(11): 476–88.
- 52Wang L, Wu D, Cheng YG, Xu JW, Chu HB, Zhang GY, et al. Warshaw technique in laparoscopic spleen-preserving distal pancreatectomy: surgical strategy and late outcomes of splenic preservation. Biomed Res Int. 2019; 2019:4074369.
- 53Suzuki O, Tanaka E, Hirano S, Suzuoki M, Hashida H, Ichimura T, et al. Efficacy of the electrothermal bipolar vessel sealer in laparoscopic spleen-preserving distal pancreatectomy with conservation of the splenic artery and vein. J Gastrointest Surg. 2009; 13: 155–8.
- 54Kim S, Yoon YS, Han HS, Cho JY, Choi Y, Hyun IG, et al. A blunt dissection technique using the LigaSure vessel-sealing device improves perioperative outcomes and postoperative splenic-vessel patency after laparoscopic spleen- and splenic-vessel-preserving distal pancreatectomy. Surg Endosc. 2018; 32: 2550–8.
- 55Guerrini GP, Lauretta A, Belluco C, Olivieri M, Forlin M, Basso S, et al. Robotic versus laparoscopic distal pancreatectomy: an up-to-date meta-analysis. BMC Surg. 2017; 17(1): 105.
- 56Goh BK, Chan CY, Soh HL, Lee SY, Cheow PC, Chow PK, et al. A comparison between robotic-assisted laparoscopic distal pancreatectomy versus laparoscopic distal pancreatectomy. Int J Med Robot. 2017; 13(1):e1733.
- 57Kamarajah SK, Sutandi N, Robinson SR, French JJ, White SA. Robotic versus conventional laparoscopic distal pancreatic resection: a systematic review and meta-analysis. HPB (Oxford). 2019; 21(9): 1107–18.
Citing Literature
