Laparoscopic Duodenum-Preserving Pancreatic Head Resection: A Technique for the Treatment of Benign or Low-Grade Malignant Tumors (10 Cases Report)

Abstract

Background:

Laparoscopic duodenum-preserving pancreatic head resection (LDPPHR) is a surgical procedure that involves the removal of the pancreatic head while aiming to preserve the integrity of the digestive and biliary tracts. With advancements in laparoscopic techniques, the utilization of LDPPHR has been increasing.

Methods:

We retrospectively analyzed the clinical data of 10 patients who underwent laparoscopic duodenum-preserving total pancreatic head resection (LDPPHR-t) at our center from June 2019 to October 2021. Additionally, we analyzed the use of indocyanine green (ICG) in the initial stage of LDPPHR, based on current reports.

Results:

LDPPHR-t was successfully performed in all patients. After surgery, 3 patients experienced pancreatic fistula (Grade B), 2 patients experienced bile leakage, and 2 patients experienced postoperative hemorrhage. However, no patient exhibited recurrence or required secondary surgery.

Conclusion:

LDPPHR-t is a new method for treating benign and low-grade malignant tumors in the pancreatic head. However, it is associated with a high incidence of postoperative complications. In the initial stage, the use of ICG can assist surgeons in identifying the biliary duct and pancreaticoduodenal artery arcade.

Introduction

Pancreaticoduodenectomy (PD) has been the traditional treatment modality for benign or low-grade malignant tumors located in the pancreatic head. In recent years, laparoscopic pancreaticoduodenectomy (LPD) has gained popularity due to increased experience and technological advancements. The mortality rate of LPD has decreased to less than 5% in high-volume centers.¹ Building upon LPD, there has been growing interest in laparoscopic duodenum-preserving pancreatic head resection (LDPPHR). LDPPHR offers the advantage of maintaining the integrity of the digestive and biliary tracts compared to LPD.² For benign or low-grade malignant tumors, complete removal of the lesion is curative, and minimal resection techniques preserve pancreatic function and provide distinct advantages over more extensive pancreatic resections. However, there is still a lack of large-scale reports on LDPPHR due to the limited experience and high demands of this procedure.^3–5 In this article, we report on 10 cases of laparoscopic duodenum-preserving total pancreatic head resection (LDPPHR-t).

Materials and Methods

Between June 2019 and October 2021, 40 patients were diagnosed with benign or low-grade malignant tumors located in the pancreatic head. Among them, 10 patients underwent LDPPHR-t, while 30 patients underwent LPD. All surgeries were performed by the same surgical team, and informed consent was obtained from the patients. The indications for LDPPHR-t in our center included benign tumors or low-grade malignant tumors located in the pancreatic head, such as solid pseudopapillary neoplasm, pancreatic neuroendocrine tumors, intraductal papillary mucinous neoplasm, and serous cystadenomas. Asymptomatic benign tumors with risk factors for malignancy, such as mural nodule, size ≥40 mm, rapid growth, and positive cytology, were also included.⁶

Data collection and definitions

Baseline demographics and perioperative data were collected for all patients. Perioperative data included age, gender, body mass index, American Society of Anesthesiology Score (ASA), history of upper abdominal surgery, operative resection time, estimated blood loss, and complications including postoperative pancreatic fistula (POPF), postoperative hemorrhage, bile leakage, delaying gastric emptying, abdominal infection, and 90-day mortality.

Definitions

The definitions and classification of POPF and bile leakage were based on the guidelines from the International Study Group of Pancreatic Surgery (ISGPS) and the International Study Group of Liver Surgery (ISGLS). The international classification system was adopted for grading postoperative bleeding.^7–9

Surgical procedure

Laparoscopic duodenum-preserving pancreatic head resection

The patient was positioned supine with the legs apart. The first step involved separating the gastro-colic ligament, followed by an incomplete Kocher maneuver to protect the posterior superior pancreaticoduodenal artery (PSPDA). The upper and lower margins of the pancreas were then mobilized to expose the common hepatic artery (CHA) and the superior mesenteric vein-portal vein (SMV-PV), respectively (Fig. 1).

FIG. 1.

Expose the GDA, the CHA, and PHA. CHA, common hepatic artery; GDA, gastroduodenal artery; PHA, proper hepatic artery.

The anterior superior pancreaticoduodenal artery (ASPDA) was isolated and preserved while dissecting the tissues along the CHA and gastroduodenal artery (GDA). Only branches reaching the pancreatic head were ligated. Simultaneously, a retropancreatic tunnel was created in front of the SMV. The pancreas was transected once the safety of the PV and SMV was ensured. During this process, attention was given to the main pancreatic duct (MPD) to avoid stenosis. The MPD was located and severed with scissors rather than an ultrasonic scalpel. Real-time indocyanine green (ICG) fluorescence imaging was used to identify the common bile duct (CBD) and guide pancreatic parenchymal resection while preserving the CBD intact. The intrapancreatic bile duct was exposed when the upper side of the pancreatic head was dissected (Fig. 2).

FIG. 2.

Expose the intrapancreatic bile duct. CBD, common bile duct.

Subsequently, the pancreas was removed along the left dorsal direction of the CBD. Careful transection of the uncinate and pancreatic heads was performed along the duodenum while preserving the branches of both the anterior and posterior inferior pancreaticoduodenal arteries, especially those supplying blood to the duodenum. The proximal end of the MPD was located and ligated adjacent to the ampulla. After retrieval of the specimen and lymph node samples, an intraoperative frozen section was sent for confirmation of the diagnosis, ruling out malignancy, and ensuring a negative margin (Fig. 3). Following sample removal, fluorescence cholangiography was performed to detect any suspicious bile duct injury. Finally, a pancreaticojejunostomy (duct to mucosa) was performed.

FIG. 3.

The tissue section during the procedure was exposed. AIPDA, anterior inferior pancreaticoduodenal artery; AIPDV, anterior inferior pancreaticoduodenal vein; CBD, common bile duct; MPD, main pancreatic duct; PIPDA, posterior inferior pancreaticoduodenal artery; PSPDA, posterior superior pancreaticoduodenal artery; SMV, superior mesenteric vein.

Postoperative management included routine administration of enzyme inhibitors, acid suppressants, anti-inflammatory medications, and supportive treatments such as fluid replacement. The abdominal drainage tube was removed based on the amylase levels in the drainage fluid and abdominal imaging results. If the amylase in the drainage fluid was negative and there was no significant fluid accumulation on the third day after surgery, the abdominal drainage tube was removed.

Results

A total of 10 cases of LDPPHR-t were performed in our center (Table 1). Among them, 8 were women and 2 were men. The average age was 35.20 ± 7.43 years old. The tumors had an average diameter of 5.50 cm, and preoperative serum tumor markers were within normal range. The mean surgical resection specimen time was 79.0 minutes, the average amount of bleeding was 133.0 mL, and the mean operative time was 100.40 ± 13.34 minutes. Three patients (30%) experienced postoperative POPF of grade B. Additionally, bile leakage occurred in 2 patients (20%), 1 of whom also had POPF, severe abdominal infection, and hemorrhage. The patient was treated with pancreatic enzyme inhibition, anti-inflammatory medication, and blood transfusion. Although the abdominal hemorrhage improved, pale yellow bile-like fluid appeared in the abdominal drainage fluid on the 10th day after surgery. The patient eventually received endoscopic nasobiliary drainage and had a good recovery. Intra-abdominal hemorrhage occurred in 2 patients. There were no cases of delayed gastric emptying or duodenal stenosis. However, 1 patient experienced slow intestinal peristalsis. The readmission rate within 30 days was 10%.

Table 1.

Clinical Data of Patients Undergoing Laparoscopic Duodenum-Preserving Pancreatic Head Resection

Variables	No. 1	No. 2	No. 3	No. 4	No. 5	No. 6	No. 7	No. 8	No. 9	No. 10
Sex	Female	Female	Man	Female	Female	Female	Female	Man	Man	Female
Age	35	34	32	45	32	43	23	28	34	46
History of upper abdominal surgery	No	No	No	Yes	No	No	No	No	Yes	Yes
The time of resected specimen (minutes)	84	79	67	75	93	78	60	89	100	65
The time of operation (minutes)	102	94	86	102	112	98	85	112	126	87
Tumor diameter (cm)	6	5	7	5	4	6	5	3	3	5
Pancreatic tissue residue on the duodenal side	No	No	Yes	No	No	No	Yes	No	No	No
Kocher incision	No	No	No	No	No	No	No	No	No	No
Anterior arch of pancreaticoduodenal artery preserving	Yes	No	Yes	No	No	No	No	No	No	No
Posterior arch of pancreaticoduodenal artery preserving	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes	Yes
Intraoperative blood loss (mL)	150	200	100	180	80	200	150	100	50	120
Postoperative pathological results	SCA	SPN	SCA	IPMN	SPN	SCA	SPN	pNET	pNET	SCA
Pancreatic fistula	No	B	No	No	No	No	B	B	No	No
Biliary fistula	No	Yes	No	No	No	Yes	No	No	No	No
Intra-abdominal hemorrhage	No	Yes	No	No	No	No	Yes	No	No	No
Intra-abdominal infection	No	Yes	No	No	No	No	Yes	Yes	No	No
Postoperative hospital stay (days)	10	23	10	9	8	15	14	15	8	7
Postoperative complications ≥CDIII	No	Yes	No	No	No	No	No	No	No	No

IPMN, intraductal papillary mucinous neoplasm; LDPPHR, laparoscopic duodenum-preserving pancreatic head resection; pNET, pancreatic neuroendocrine tumors; SCA, serous cystadenoma; SPN, solid pseudopaillary neoplasm.

The average length of follow-up was 28 months. All patients were regularly monitored, and none experienced recurrence or metastasis. No new onset of diabetes mellitus was observed during long-term follow-up in terms of endocrine dysfunction. However, 1 patient was diagnosed with pancreatic exocrine insufficiency after LDPPHR and required pancreatic enzyme supplementation to prevent fatty diarrhea. All patients reported a high quality of life, and no cases of biliary stricture were observed.

During the same period, the LDPPHR-t group had a significantly higher rate of postoperative complications compared to the LPD group (Table 2). There were significant differences in postoperative POPF, intraoperative blood loss (mL), and postoperative hospital stay (days) between the two groups.

Table 2.

Postoperative Complications of Patients Undergoing Laparoscopic Duodenum-Preserving Pancreatic Head Resection Compared with Laparoscopic Pancreaticoduodenectomy

Variable	LPD	LDPPHR	P
Pancreatic fistula	29/1	7/3	.015
Biliary fistula	30/0	8/2	.012
Intra-abdominal hemorrhage	27/3	8/2	.408
Intraoperative blood loss (mL)	222.67 ± 67.95	133.00 ± 51.43	<.001
Intra-abdominal infection	29/1	7/3	.015
Postoperative hospital stay (days)	16.80 ± 4.77	11.90 ± 4.91	.008
Postoperative complications ≥CDIII	28/2	9/1	.729

LPD, laparoscopic pancreaticoduodenectomy.

Discussion

LDPPHR offers several advantages over LPD, including preservation of the integrity of the digestive tract and biliary system, reduced trauma, and improved quality of life. LDPPHR is also beneficial for maintaining pancreatic exocrine and endocrine function and better regulation of glucose metabolism.¹⁰ Some studies have reported significant long-term advantages of LDPPHR over LPD.^11,12 Beger et al. suggested that DPPHR is associated with a low level of early postoperative complications and better preservation of exocrine and endocrine functions.¹³ However, LDPPHR requires more team cooperation and is more technically demanding compared to LPD. Based on our experience with LPD, we have performed 10 LDPPHR cases. In this article, we have discussed the important aspects of performing LDPPHR based on our experience.

Management of the pancreasduodenal arterial circle

Preserving an adequate blood supply to the duodenum and terminal bile duct is crucial in LDPPHR to avoid ischemia. The pancreasduodenal arterial circle consists of four arteries: the ASPDA, anterior inferior pancreaticoduodenal artery (AIPDA), PSPDA, and posterior inferior pancreaticoduodenal artery (PIPDA). The PSPDA, PIPDA, and AIPDA are essential for maintaining blood flow to the intrapancreatic section of the CBD. The blood supply to the duodenal papilla is mainly maintained by the PSPDA.¹¹ Surgeons performing LDPPHR should be familiar with the anatomy of the pancreatic head region, especially the location of these blood vessels. It is particularly important to protect the PSPDA and PIPDA. According to Cao's report, the ASPDA and AIPDA are often located in the pancreatic capsule, ∼0.5 to 1.5 cm from the margin of the duodenum.¹⁴ When creating a gap between the horizontal portion of the duodenum and the pancreas, the pancreatic capsule should be completely closed to preserve the ASPDA and AIPDA. The PSPDA and PIPDA are found in the posterior mesangium of the pancreas, around 1.5–2.0 cm from the margin of the duodenum.

Therefore, to protect these arteries, we do not perform a Kocher maneuver. We believe that it can disrupt the blood flow to the lateral duodenum and posterior peritoneum, and it is of little importance in laparoscopic surgery. Although there were 2 patients in whom the anterior arch was not preserved, they both recovered well without duodenal or biliary ischemia. To safeguard the posterior arch, the GDA was dissected along the CHA, and then the anterior and posterior branches of the superior pancreaticoduodenal artery were separated in our center.

Protection of the common bile duct and management of the pancreatic duct

The PSPDA typically begins in front of the CBD, travels to the right side of the CBD, and supplies blood to the duodenal papilla. The pancreatic duct was isolated along the ampulla and then ligated. When dissociating the intrapancreatic bile duct, care must be taken not to injure the bile duct.¹⁵ Excessive removal of pancreatic tissue behind the bile duct is a risk factor for postoperative bile leakage, as it can cause bile duct ischemia. Therefore, it is not necessary to excessively remove extra pancreatic tissue around the bile duct, as it can avoid damage to the bile duct and reduce the impact on its blood supply. In the initial stage, ICG fluorescence can be used to identify the bile duct (Fig. 4).

FIG. 4.

During surgery, ICG is used to identify the biliary tract. CBD, common bile duct; ICG, indocyanine green.

ICG can not only identify the biliary tract but also detect postoperative bile leakage.^16,17 Attention should also be paid to the occurrence of delayed bile leakage. Adequate drainage is crucial to prevent postoperative POPF. To avoid damage to the bile duct and prevent compression of the biliary tract, the drainage tube should be carefully placed. Some reports suggest that biliary drainage can reduce bile duct pressure, support the bile duct to prevent postoperative stenosis, and decrease bile flow into the duodenum to reduce duodenal pressure, especially in cases of postoperative pancreatic leakage. This can effectively prevent the activation of pancreatic juice, reducing the rate of postoperative infection and bleeding.¹⁸ If there is a small breach in the bile duct wall, most cases can be improved with adequate biliary drainage and anti-infection treatment.

However, endoscopic retrograde cholangiopancreatography can be considered for patients with a large volume of drainage. Traditional Beger surgery preserves a part of the pancreatic tissue, which can increase the incidence of POPF⁴; therefore, to reduce the incidence of POPF, we advocate total pancreatic head resection. The incidence of postoperative complications such as POPF in our center was higher compared to the reported rates by Peng et al. This may be attributed to the fact that our center has performed fewer cases of LPDDHR and is currently in the learning curve phase.⁴

Compared to LPD, LDPPHR has demonstrated significant advantages in reducing long-term endocrine and exocrine functional impairments, while also preserving the integrity of the gastrointestinal and biliary tracts. However, it is important to note that LDPPHR carries a higher risk of postoperative complications such as POPF and biliary-related issues, as indicated by previous studies.¹⁹ On the other hand, patients who underwent LDPPHRt reported a higher quality of life following the procedure.²⁰ The successful execution of LDPPHR requires a more meticulous surgical technique and a higher level of teamwork. Consequently, the development of expertise in LDPPHR may necessitate a longer learning period for surgeons to acquire the necessary skills and proficiency. Therefore, it is highly recommended that the performance of LDPPHR be exclusively conducted in surgical centers with extensive experience in both LPD and DPPHRt.²⁰

Biliary fistula is one of the most common postoperative complications of LDPPHR, with a prevalence of 4.5%–16.7%.^4,21 Furthermore, research has shown that LDPPHR can reduce long-term endocrine and exocrine dysfunction. In our center, the incidence of biliary fistula was ∼20%, and the incidence of exocrine dysfunction was ∼10%.

Footnotes

Acknowledgment

We thank Y.F. who came up with the idea.

Authors' Contributions

Conception and design: Y.L., S.W., X.L. Data analysis and interpretation: Y.F. and Y.G. Manuscript writing: All authors. Final approval of manuscript: All authors.

Consent for Publication

All authors agreed to publish this article.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Wang

, Peng

, Liu

, et al. Practice patterns and perioperative outcomes of laparoscopic pancreaticoduodenectomy in China: A retrospective multicenter analysis of 1029 patients. Ann Surg, 2021; 273(1):145–153; doi: 10.1097/SLA.0000000000003190. PMID: 30672792.

Peng

, Shen

, Deng

, et al. Early experience for the robotic duodenum-preserving pancreatic head resection. World J Surg, 2012; 36(5):1136–1141; doi: 10.1007/s00268-012-1503-6

Liang

, Chen

, Li

, et al. Total laparoscopic duodenum-preserving pancreatic head resection for solid pseudopaillary neoplasm of pancreas: A case report. Medicine (Baltimore), 2019; 98(21):e15823; doi: 10.1097/MD.0000000000015823

Cao

, Li

, Wei

, et al. Laparoscopic duodenum-preserving total pancreatic head resection: A novel surgical approach for benign or low-grade malignant tumors. Surg Endosc, 2019; 33(2):633–638; doi: 10.1007/s00464-018-6488-2

Cai

, Zheng

, Gao

, et al. Laparoscopic duodenum-preserving total pancreatic head resection using real-time indocyanine green fluorescence imaging. Surg Endosc, 2021; 35(3):1355–1361; doi: 10.1007/s00464-020-07515-6

European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut, 2018; 67,(5):789–804.

Bassi

, Marchegiani

, Dervenis

, 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.

Koch

, Garden

, Padbury

, et al. Bile leakage after hepatobiliary and pancreatic surgery: A definition and grading of severity by the International Study Group of Liver Surgery. Surgery, 2011; 149,(5):680–688.

Wente

, Veit

, Bassi

, et al. Postpancreatectomy hemorrhage (PPH): An International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery, 2007; 142,(1):20–25.

10.

Diener

, Hüttner

, Kieser

, et al. Partial pancreatoduodenectomy versus duodenum-preserving pancreatic head resection in chronic pancreatitis: the multicentre, randomised, controlled, double-blind ChroPac trial. Lancet, 2017; 390(10099):1027–1037; doi: 10.1016/S0140-6736(17)31960-8

11.

Beger

, Schwarz

, Poch

. Duodenum-preserving total pancreatic head resection for benign cystic neoplastic lesions. J Gastrointest Surg, 2012; 16(11):2160–2166; doi: 10.1007/s11605-012-1929-z

12.

Beger

, Siech

, Poch

. Duodenum-preserving total pancreatic head resection: An organ-sparing operation technique for cystic neoplasms and non-invasive malignant tumors. Chirurg, 2013; 84(5):412–420; doi: 10.1007/s00104-012-2423-6

13.

Beger

, Nakao

, Mayer

, et al. Duodenum-preserving total and partial pancreatic head resection for benign tumors—Systematic review and meta-analysis. Pancreatology, 2015; 15(2):167–178; doi: 10.1016/j.pan.2015.01.009

14.

Kumar

, Garg

, Yadav

, et al. Anatomy of peripancreatic arteries and pancreaticoduodenal arterial arcades in the human pancreas: A cadaveric study. Surg Radiol Anat, 2021; 43(3):367–375; doi: 10.1007/s00276-020-02632-2

15.

Tsuchikawa

, Hirano

, Tanaka

, et al. Modified duodenum-preserving pancreas head resection for low-grade malignant lesion in the pancreatic head. Pancreatology, 2013; 13(2):170–174; doi: 10.1016/j.pan.2012.12.001

16.

Chen

, Gao

, Cai

, et al. Indocyanine green-enhanced fluorescence in laparoscopic duodenum-preserving pancreatic head resection: Technique with video. Ann Surg Oncol, 2020; 27(10):3926–3927; doi: 10.1245/s10434-020-08360-6

17.

Kapoor

, Nundy

. Bile duct leaks from the intrahepatic biliary tree: A review of its etiology, incidence, and management. HPB Surg, 2012; 2012:752932; doi: 10.1155/2012/752932

18.

Chen

, Peng

, Chen

, et al. Laparoscopic resection of duodenal and pancreatic head: Experience in four cases. Chin J Hepatobil Surg, 2019; 25,(10):755–758.

19.

Beger

, Mayer

, Poch

. Resection of the duodenum causes long-term endocrine and exocrine dysfunction after Whipple procedure for benign tumors-results of a systematic review and meta-analysis. HPB, 2020; 22(6):809–820; doi: 10.1016/j.hpb.2019.12.016

20.

Liu

, Peng

. Laparoscopic duodenum-preserving total pancreatic-head resection versus standard pancreaticoduodenectomy for pancreatic-head intraductal papillary mucinous neoplasm. Asian J Surg, 2023; 46(6):2293–2298; doi: 10.1016/j.asjsur.2022.09.108

21.

Jiang

, Jin

, Zhan

, et al. Robot-assisted duodenum-preserving pancreatic head resection with pancreaticogastrostomy for benign or premalignant pancreatic head lesions: A single-centre experience. Int J Med Robot, 2018; 14(4):e1903; doi: 10.1002/rcs.1903