Comparison of perioperative outcomes between laparoscopic duodenum-preserving pancreatic head resection and minimally invasive enucleation for benign or low-grade malignant tumors of the pancreatic head with main pancreatic duct involvement_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LI Zheng , SHI Yihua , LIU Wensheng , ZHUO Qifeng , JI Shunrong , ZHOU Chenjie , YU Xianjun ,  XU Xiaowu

Department of Pancreatic Surgery, Fudan University Shanghai Cancer Center; Department of Oncology, Shanghai Medical College, Fudan University; Shanghai Pancreatic Cancer Institute; Shanghai Key Laboratory of Precision Medicine for Pancreatic Cancer; Pancreatic Cancer Institute, Fudan University, Shanghai 200032, P. R. China;

Corresponding author：

XU Xiaowu, Email: xuxiaowu@fudanpci.org

Keywords：

pancreatic head tumor; laparoscopic duodenum-preserving pancreatic head resection; minimally invasive enucleation; main pancreatic duct repair and reconstruction; perioperative prognosis

DOI：

10.7507/1007-9424.202501036

Video：

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Objective To compare the perioperative outcomes of laparoscopic duodenum-preserving pancreatic head resection (LDPPHR) and minimally invasive enucleation (MIEN) in the treatment of benign or low-grade malignant tumors of the pancreatic head. Methods A retrospective analysis was conducted on the clinical data of patients who underwent LDPPHR (n=30) and MIEN (n=38) at Fudan University Shanghai Cancer Center between March 2021 and November 2024. The perioperative outcomes of the LDPPHR and MIEN groups were compared. Preoperative assessment of tumors in the MIEN group showed that they were partially or completely encircling the main pancreatic duct. Results The MIEN group had a significantly shorter operative time compared to the LDPPHR group (229.0 min vs. 388.5 min, P<0.001), with less intraoperative blood loss (100.0 mL vs. 200.0 mL, P=0.028). Regarding the management of the main pancreatic duct, 26.3% (10/38) of patients in the MIEN group had an intact and unexposed main pancreatic duct, 10.5% (4/38) had exposed but undamaged ducts, 7.9% (3/38) had duct injury repaired with simple suture, and 55.3% (21/38) required stenting for duct repair and reconstruction following injury. Although the incidence of postoperative pancreatic fistula was higher in the MIEN group compared to the LDPPHR group [grade B: 73.7% (28/38) vs. 43.3% (13/30)], no significant differences were observed between the two groups in other perioperative outcomes (such as postoperative length of stay, discharge rate with drainage tube, and Clavien-Dindo complication grading, all P>0.05). One patient in the MIEN group required reoperation due to early postoperative hemorrhage. Conclusions MIEN is a feasible surgical option for treating benign or low-grade malignant pancreatic head tumors with involvement of the main pancreatic duct. It shows significant advantages, particularly in terms of preserving organ function and maintaining normal anatomical structures. Despite the higher incidence of pancreatic fistula, no significant differences were observed in other perioperative outcomes compared to LDPPHR. Therefore, MIEN holds great promise in the treatment of pancreatic head tumors, especially for younger patients with a strong desire for function preservation.

Citation： LI Zheng, SHI Yihua, LIU Wensheng, ZHUO Qifeng, JI Shunrong, ZHOU Chenjie, YU Xianjun, XU Xiaowu. Comparison of perioperative outcomes between laparoscopic duodenum-preserving pancreatic head resection and minimally invasive enucleation for benign or low-grade malignant tumors of the pancreatic head with main pancreatic duct involvement. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2025, 32(2): 156-162. doi: 10.7507/1007-9424.202501036 Copy

1.	Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J Am Coll Surg, 2015, 220(4): 530-536.
2.	Beger HG, Poch B, Mayer B, et al. New onset of diabetes and pancreatic exocrine insufficiency after pancreaticoduodenectomy for benign and malignant tumors: a systematic review and meta-analysis of long-term results. Ann Surg, 2018, 267(2): 259-270.
3.	李征, 刘文生, 史逸华, 等. 困难腹腔镜根治性顺行模块化胰脾切除术的处理要点与思考. 中国普外基础与临床杂志, 2023, 30(11): 1284-1288.
4.	Beger HG, Mayer B, Rau BM. Parenchyma-sparing, limited pancreatic head resection for benign tumors and low-risk periampullary cancer–a systematic review. J Gastrointest Surg, 2016, 20(1): 206-217.
5.	Beger HG, Mayer B, Vasilescu C, et al. Long-term metabolic morbidity and steatohepatosis following standard pancreatic resections and parenchyma-sparing, local extirpations for benign tumor: a systematic review and meta-analysis. Ann Surg, 2022, 275(1): 54-66.
6.	刘文生, 卓奇峰, 吉顺荣, 等. 保留胰管的胰腺部分切除术. 中国普外基础与临床杂志, 2022, 29(3): 281-284.
7.	Bolm L, Nebbia M, Wei AC, et al. Long-term outcomes of parenchyma-sparing and oncologic resections in patients with nonfunctional pancreatic neuroendocrine tumors <3 cm in a large multicenter cohort. Ann Surg, 2022, 276(3): 522-531.
8.	Beger HG, Krautzberger W, Bittner R, et al. Duodenum-preserving resection of the head of the pancreas in patients with severe chronic pancreatitis. Surgery, 1985, 97(4): 467-473.
9.	Kato H, Isaji S, Azumi Y, et al. Development of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH) after pancreaticoduodenectomy: proposal of a postoperative NAFLD scoring system. J Hepatobiliary Pancreat Sci, 2010, 17(3): 296-304.
10.	Kato H, Asano Y, Ito M, et al. Significant positive impact of duodenum-preserving pancreatic head resection on the prevention of postoperative nonalcoholic fatty liver disease and acute cholangitis. Ann Gastroenterol Surg, 2022, 6(6): 851-861.
11.	Umemoto K, Tsuchikawa T, Nakamura T, et al. Postoperative nutritional benefits of proximal parenchymal pancreatectomy for low-grade malignant lesions in the pancreatic head. HPB (Oxford), 2019, 21(11): 1491-1496.
12.	Beger HG, Mayer B, Poch B. Long-term oncologic outcome following duodenum-preserving pancreatic head resection for benign tumors, cystic neoplasms, and neuroendocrine tumors: systematic review and meta-analysis. Ann Surg Oncol, 2024, 31(7): 4637-4653.
13.	Polanco PM, Karalis JD, Abreu AA, et al. Robotic enucleation of pancreatic head insulinomas in close proximity to the pancreatic duct. Ann Surg Oncol, 2024, 31(3): 1834. doi: 10.1245/s10434-023-14627-5.
14.	Tang W, Gao Y, Zhao Z, et al. Intraoperative ultrasound guided robotic pancreatic enucleation, does a distance of 3 mm still matters? Surg Innov, 2023, 30(2): 166-175.
15.	Li Z, Zhuo Q, Shi Y, et al. Minimally invasive enucleation of pancreatic tumors: the main pancreatic duct is no longer a restricted area. Heliyon, 2023, 9(11): e21917. doi: 10.1016/j.heliyon.2023.e21917.
16.	Tanaka M, Fernández-Del Castillo C, Kamisawa T, et al. Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas. Pancreatology, 2017, 17(5): 738-753.
17.	European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut, 2018, 67(5): 789-804.
18.	Marchegiani G, Salvia R, Verona EBM 2020 on IPMN. Guidelines on pancreatic cystic neoplasms: major inconsistencies with available evidence and clinical practice- results from an international survey. Gastroenterology, 2021, 160(7): 2234-2238.
19.	Peng F, He R, Wang H, et al. Development of a difficulty scoring system for laparoscopic pancreatoduodenectomy in the initial stage of the learning curve: a retrospective cohort study. Int J Surg, 2023, 109(4): 660-669.
20.	Zhou M, Xu S, Chao D, et al. Intracapsular approach used in laparoscopic duodenum-preserving total pancreatic head resection for pancreatic head benign or low-grade malignant tumors. Langenbecks Arch Surg, 2022, 407(8): 3851-3858.
21.	Cai Y, Zheng Z, Gao P, et al. Laparoscopic duodenum-preserving total pancreatic head resection using real-time indocyanine green fluorescence imaging. Surg Endosc, 2021, 35(3): 1355-1361.
22.	Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6 336 patients and results of a survey. Ann Surg, 2004, 240(2): 205-213.
23.	Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery, 2017, 161(3): 584-591.
24.	Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery, 2007, 142(1): 20-25.
25.	Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery, 2007, 142(5): 761-768.
26.	Beger HG, Mayer B, Poch B. Duodenum-preserving pancreatic head resection for benign and premalignant tumors-a systematic review and meta-analysis of surgery-associated morbidity. J Gastrointest Surg, 2023, 27(11): 2611-2627.
27.	Yin T, Wen J, Zhen T, et al. Long-term quality of life between duodenum-preserving pancreatic head resection and pancreatoduodenectomy: a systematic review and meta-analysis. Int J Surg, 2024, 110(2): 1139-1148.
28.	Cuschieri A. Reducing errors in the operating room: surgical proficiency and quality assurance of execution. Surg Endosc, 2005, 19(8): 1022-1027.
29.	Pedrazzoli S, Canton SA, Sperti C. Duodenum-preserving versus pylorus-preserving pancreatic head resection for benign and premalignant lesions. J Hepatobiliary Pancreat Sci, 2011, 18(1): 94-102.
30.	Fischer TD, Gutman DS, Warner EA, et al. Local pancreatic head resection: the search for optimal indications through quality of life assessments. Am J Surg, 2015, 210(3): 417-423.
31.	Finney JM. Ⅶ. Resection of the pancreas: report of a case. Ann Surg, 1910, 51(6): 818-829.
32.	Ramesh H. End-to-end anastomosis of pancreas. Surgery, 2002, 131(6): 691-693.
33.	Kokudo T, Petermann D, Demartines N, et al. Laparoscopic pancreatic enucleation with end-to-end pancreatic duct reconstruction. Ann Surg Oncol, 2015, 22(4): 1190. doi: 10.1245/s10434-014-4188-2.
34.	Liu R, Liu Q. Pancreatic duct surgery: from innovation to implementation. Intell Surg, 2023, 6: 8-11.

1. Cameron JL, He J. Two thousand consecutive pancreaticoduodenectomies. J Am Coll Surg, 2015, 220(4): 530-536.
2. Beger HG, Poch B, Mayer B, et al. New onset of diabetes and pancreatic exocrine insufficiency after pancreaticoduodenectomy for benign and malignant tumors: a systematic review and meta-analysis of long-term results. Ann Surg, 2018, 267(2): 259-270.
3. 李征, 刘文生, 史逸华, 等. 困难腹腔镜根治性顺行模块化胰脾切除术的处理要点与思考. 中国普外基础与临床杂志, 2023, 30(11): 1284-1288.
4. Beger HG, Mayer B, Rau BM. Parenchyma-sparing, limited pancreatic head resection for benign tumors and low-risk periampullary cancer–a systematic review. J Gastrointest Surg, 2016, 20(1): 206-217.
5. Beger HG, Mayer B, Vasilescu C, et al. Long-term metabolic morbidity and steatohepatosis following standard pancreatic resections and parenchyma-sparing, local extirpations for benign tumor: a systematic review and meta-analysis. Ann Surg, 2022, 275(1): 54-66.
6. 刘文生, 卓奇峰, 吉顺荣, 等. 保留胰管的胰腺部分切除术. 中国普外基础与临床杂志, 2022, 29(3): 281-284.
7. Bolm L, Nebbia M, Wei AC, et al. Long-term outcomes of parenchyma-sparing and oncologic resections in patients with nonfunctional pancreatic neuroendocrine tumors <3 cm in a large multicenter cohort. Ann Surg, 2022, 276(3): 522-531.
8. Beger HG, Krautzberger W, Bittner R, et al. Duodenum-preserving resection of the head of the pancreas in patients with severe chronic pancreatitis. Surgery, 1985, 97(4): 467-473.
9. Kato H, Isaji S, Azumi Y, et al. Development of nonalcoholic fatty liver disease (NAFLD) and nonalcoholic steatohepatitis (NASH) after pancreaticoduodenectomy: proposal of a postoperative NAFLD scoring system. J Hepatobiliary Pancreat Sci, 2010, 17(3): 296-304.
10. Kato H, Asano Y, Ito M, et al. Significant positive impact of duodenum-preserving pancreatic head resection on the prevention of postoperative nonalcoholic fatty liver disease and acute cholangitis. Ann Gastroenterol Surg, 2022, 6(6): 851-861.
11. Umemoto K, Tsuchikawa T, Nakamura T, et al. Postoperative nutritional benefits of proximal parenchymal pancreatectomy for low-grade malignant lesions in the pancreatic head. HPB (Oxford), 2019, 21(11): 1491-1496.
12. Beger HG, Mayer B, Poch B. Long-term oncologic outcome following duodenum-preserving pancreatic head resection for benign tumors, cystic neoplasms, and neuroendocrine tumors: systematic review and meta-analysis. Ann Surg Oncol, 2024, 31(7): 4637-4653.
13. Polanco PM, Karalis JD, Abreu AA, et al. Robotic enucleation of pancreatic head insulinomas in close proximity to the pancreatic duct. Ann Surg Oncol, 2024, 31(3): 1834. doi: 10.1245/s10434-023-14627-5.
14. Tang W, Gao Y, Zhao Z, et al. Intraoperative ultrasound guided robotic pancreatic enucleation, does a distance of 3 mm still matters? Surg Innov, 2023, 30(2): 166-175.
15. Li Z, Zhuo Q, Shi Y, et al. Minimally invasive enucleation of pancreatic tumors: the main pancreatic duct is no longer a restricted area. Heliyon, 2023, 9(11): e21917. doi: 10.1016/j.heliyon.2023.e21917.
16. Tanaka M, Fernández-Del Castillo C, Kamisawa T, et al. Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas. Pancreatology, 2017, 17(5): 738-753.
17. European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut, 2018, 67(5): 789-804.
18. Marchegiani G, Salvia R, Verona EBM 2020 on IPMN. Guidelines on pancreatic cystic neoplasms: major inconsistencies with available evidence and clinical practice- results from an international survey. Gastroenterology, 2021, 160(7): 2234-2238.
19. Peng F, He R, Wang H, et al. Development of a difficulty scoring system for laparoscopic pancreatoduodenectomy in the initial stage of the learning curve: a retrospective cohort study. Int J Surg, 2023, 109(4): 660-669.
20. Zhou M, Xu S, Chao D, et al. Intracapsular approach used in laparoscopic duodenum-preserving total pancreatic head resection for pancreatic head benign or low-grade malignant tumors. Langenbecks Arch Surg, 2022, 407(8): 3851-3858.
21. Cai Y, Zheng Z, Gao P, et al. Laparoscopic duodenum-preserving total pancreatic head resection using real-time indocyanine green fluorescence imaging. Surg Endosc, 2021, 35(3): 1355-1361.
22. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6 336 patients and results of a survey. Ann Surg, 2004, 240(2): 205-213.
23. Bassi C, Marchegiani G, Dervenis C, et al. The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery, 2017, 161(3): 584-591.
24. Wente MN, Veit JA, Bassi C, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery, 2007, 142(1): 20-25.
25. Wente MN, Bassi C, Dervenis C, et al. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery, 2007, 142(5): 761-768.
26. Beger HG, Mayer B, Poch B. Duodenum-preserving pancreatic head resection for benign and premalignant tumors-a systematic review and meta-analysis of surgery-associated morbidity. J Gastrointest Surg, 2023, 27(11): 2611-2627.
27. Yin T, Wen J, Zhen T, et al. Long-term quality of life between duodenum-preserving pancreatic head resection and pancreatoduodenectomy: a systematic review and meta-analysis. Int J Surg, 2024, 110(2): 1139-1148.
28. Cuschieri A. Reducing errors in the operating room: surgical proficiency and quality assurance of execution. Surg Endosc, 2005, 19(8): 1022-1027.
29. Pedrazzoli S, Canton SA, Sperti C. Duodenum-preserving versus pylorus-preserving pancreatic head resection for benign and premalignant lesions. J Hepatobiliary Pancreat Sci, 2011, 18(1): 94-102.
30. Fischer TD, Gutman DS, Warner EA, et al. Local pancreatic head resection: the search for optimal indications through quality of life assessments. Am J Surg, 2015, 210(3): 417-423.
31. Finney JM. Ⅶ. Resection of the pancreas: report of a case. Ann Surg, 1910, 51(6): 818-829.
32. Ramesh H. End-to-end anastomosis of pancreas. Surgery, 2002, 131(6): 691-693.
33. Kokudo T, Petermann D, Demartines N, et al. Laparoscopic pancreatic enucleation with end-to-end pancreatic duct reconstruction. Ann Surg Oncol, 2015, 22(4): 1190. doi: 10.1245/s10434-014-4188-2.
34. Liu R, Liu Q. Pancreatic duct surgery: from innovation to implementation. Intell Surg, 2023, 6: 8-11.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Comparison of perioperative outcomes between laparoscopic duodenum-preserving pancreatic head resection and minimally invasive enucleation for benign or low-grade malignant tumors of the pancreatic head with main pancreatic duct involvement

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