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Chin Med J (Engl)
Chin Med J (Engl)
CM9
Chinese Medical Journal
0366-6999
2542-5641
Lippincott Williams & Wilkins Hagerstown, MD

CMJ-2023-3196
10.1097/CM9.0000000000003285
00011
3
Correspondence
Main duct-first approach: A potential expansion of indications for pancreatic enucleation in benign and low-grade malignant lesions
Wang Xing 1
Fu Xiang 2
Chen Yonghua 1
Zhang Hao 1
Zheng Zhenjiang 1
Zhong Xiaofei 3
Wang Rui 4
Liu Xubao 1
Tan Chunlu 1
Gao Ting
1 Department of General Surgery, Division of Pancreatic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, China
2 Department of General Surgery, Chongqing General Hospital, Chongqing University, Chongqing 400013, China
3 Department of Ultrasound Medicine, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, China
4 Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, China
Correspondence to: Chunlu Tan, Department of General Surgery, Division of Pancreatic Surgery, West China Hospital, Sichuan University, No 37, Guo Xue Alley, Chengdu, Sichuan 610041, China E-Mail: chunlutan@163.com
20 8 2024
20 9 2024
137 18 22362238
12 2 2024
Copyright © 2024 The Chinese Medical Association, produced by Wolters Kluwer, Inc. under the CC-BY-NC-ND license.
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. http://creativecommons.org/licenses/by-nc-nd/4.0

OPEN-ACCESSTRUE
SDCT
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pmcTo the Editor: Pancreatoduodenectomy (PD), distal pancreatectomy (DP), and central pancreatectomy (CP) usually lead to an undesirable loss of functional pancreatic parenchyma, disruption of the continuity of the digestive tract, and high incidence of complications. In recent years, traditional pancreatic enucleation (TPE) has been increasingly performed for small benign and low-grade malignant pancreatic lesions >2 mm away from the main duct (MD) as it can maximize the preservation of functional pancreatic parenchyma and retain the continuity of the digestive tract. Cases with a too short distance (≤2 mm) are not good candidates, as a too short distance may damage the MD when TPE is performed.[1] Herein, a novel pancreatic enucleation procedure, the main-duct-first approach pancreatic enucleation (MDFAPE), was introduced for small benign and low-grade malignant lesions ≤2 mm away from the MD.

This study was approved by the Ethical Review Board of the West China Hospital, Sichuan University (No. 2023[52]). Informed consent was obtained from all the participants. Informations from patients with pathologically confirmed benign or low-grade malignant tumors who underwent TPE or MDFAPE in the department of pancreatic surgery from January 2020 to April 2022 were retrieved from the database of West China Hospital. Preoperative diagnosis and the assessment of the distance between the lesion and the MD was determined by a radiologist and an experienced surgeon based on contrast-enhanced computed tomography (CT) and magnetic resonance imaging (MRI), with the addition of a sonographer based on upper digestive endoscopic ultrasonography (EUS) when distance ≤2 mm was suspected. TPE or MDFAPE was performed for patients with presumed benign or low-grade malignant tumors. TPE was performed only in cases in which the tumor margin was >2 mm away from the MD. MDFAPE was performed only in cases in which the tumor margin was ≤2 mm away from the MD.

TPE is a traditional technique, which has been described in our previous study.[2] For MDFAPE, an intraoperative ultrasound test was performed routinely to explore the tumor and its relationship with the MD, and different surgical techniques were adopted for tumors based on their location and morphology. For a solid or cystic tumor located deep in the pancreatic neck, body, or in the partition of the pancreatic head next to the neck [Figure 1A, B], firstly, the distal section of the MD was chosen to be exposed if it was dilated by the obstruction of the tumor; otherwise, the proximal section of the MD was chosen because it is generally wider than the distal section. Secondly, a plane was developed close to the margin of the tumor (if it was a cystic tumor), or about 3 mm away from the tumor margin (if it was a solid tumor, as the solid tumor always did not have a clear margin and complete envelope) to separate them from the anterior side to the posterior side until the MD was identified and protected. After confirming the integrity of the MD, the tumor was completely separated from the pancreas and removed [Figure 1D, E].

Figure 1 The preoperative and intraoperative imaging in the MDFAPE group. Green and blue arrows indicate the tumor and MD, respectively. (A) Cystic tumor in the pancreatic neck; (B) Solid tumor in the pancreatic neck; (C) Cystic tumor in the part of the pancreatic head next to the duodenum; the yellow arrow shows the duodenum; (D) The green arrow shows the cystic tumor located in the pancreatic neck, the blue arrow shows the MD; (E) The green arrow shows the solid tumor located in the pancreatic neck, the blue arrow shows the MD; (F) The blue arrow shows the MD after the cystic tumor located in the part of the pancreatic head that was next to the duodenum was removed, the yellow dashed line indicates that the dissection started from the uncinate process of pancreas until the ampulla of Vater was found, and the black arrow shows the ampulla of Vater. MD: Main duct; MDFAPE: Main-duct-first approach pancreatic enucleation.

For tumors located in the part of the pancreatic head next to the duodenum [Figure 1C], the uncinate process of the pancreas was carefully separated from its posterior attachments to expose the ampulla of Vater, while injury to the inferior pancreaticoduodenal artery was avoided. The pancreatic tissue was then separated from cephalad to caudad along the sphincter to expose the MD. After that, the tumor together with the pancreatic tissue surrounding it was separated along the MD until it was completely free and removed [Figure 1F]. The tubular tissue was not ligated until its nature was confirmed during the process of separating the pancreatic tissue, because the MD might become spastic and thin (approximately less than 1 mm in diameter) due to stimulation and be misidentified as a branch duct and ligated. After the tumor was removed, if injury to the MD was suspected, the integrity of the MD was confirmed by intraoperative ultrasound.

Continuous variables with normal distribution are presented as mean ± standard deviation (SD) or range, and were compared using Student’s t-test. Categorical variables are presented as numbers (percentages), and were compared using the Pearson χ2 test or Fisher’s exact test in cases with a expectation <5. A 1:2 propensity score matching (PSM) was used to balance the baseline data between the two groups that could influence the surgical outcomes, especially for tumor site, tumor size, and cystic morphology, which have been reported to be risk factors for postoperative pancreatic fistula (POPF) after enucleation.[2] All statistical analyses were performed using SPSS. 22 software (IBM Corp., Armonk, NY, USA).

The baseline characteristics before and after PSM are shown in Supplementary Table 1, http://links.lww.com/CM9/C132. From January 2020 to April 2022, MDFAPE and TPE were performed on 21 and 77 patients, respectively. After matching, no case in the MDFAPE group was lost; 39 cases in the TPE group were matched. All the cases achieved R0 margins. The short-term surgical outcomes are summarized in Supplementary Table 2, http://links.lww.com/CM9/C132. The most common indication for MDFAPE and TPE was pancreatic cystic neoplasm (52.4% [11/21] vs. 51.3% [20/39], respectively), followed by pancreatic neuroendocrine tumors (pNET; 38.1% [8/21] vs. 35.9% [14/39]). The clinical POPF rate was significantly higher in the MDFAPE group (66.7% [14/21] vs. 15.4% [6/39], χ2 = 16.154, P <0.001). Thirteen cases out of 21 were grade B POPF in the MDFAPE group, and 12 of these only resulted in a drain removal time longer than three weeks postoperatively. Of note, one patient (4.8%) in the MDFAPE group developed grade C POPF due to recurrent episodes of pancreatitis caused by MD stenosis postoperatively, and underwent reoperation of pancreaticojejunostomy more than seven weeks after primary surgery. In the TPE group, five cases (12.8%) out of 39 had grade B POPF, and one (2.5%) case had grade C POPF due to intraperitoneal hemorrhage and abscess, which required reoperation.

However, compared with TPE, MDFAPE did not lead to significantly more severe complications (≥Clavien-Dindo Grade III) (9.5% [2/21] vs. 5.1% [2/39], χ2 = 0.424, P = 0.515). There were two cases of Clavien-Dindo Grade III morbidity identified in both the TPE and MDFAPE groups, while Grade IV and V morbidity was not observed in the two groups. One patient in the MDFAPE group required interventional therapy to stop bleeding due to intraperitoneal hemorrhage on the second day after laparoscopic surgery and the other patient required reoperation for postoperative MD stenosis. Additionally, there were no significant differences between the MDFAPE and TPE groups in terms of the operative time (182.9 min vs. 161.5 min, t = −1.742, P = 0.087), blood loss (48.6 mL vs. 39.7 mL, t = −0.884, P = 0.380), postoperative hemorrhage rate (4.8% [1/21] vs. 5.1% [2/39], χ2 = 0.004, P = 0.950), reoperation rate (4.8% [1/21] vs. 2.5% [1/39], χ2 = 0.205, P = 0.651), and readmission rate (4.8% [1/21] vs. 0, χ2 = 1.889, P = 0.169). The postoperative hospital stay was longer in the MDFAPE group than in the TPE group (15.0 days vs. 9.8 days, t = −3.142, P = 0.003), and laparoscopic procedures were performed more frequently in the TPE group than in the MDFAPE group (51.3% [20/39] vs. 9.5% [2/21], χ2 = 10.250, P = 0.001).

As a too short distance is between the lesion and the MD may damage the latter when PE is performed, some researchers proposed the preoperative placement of a pancreatic duct stent for these cases, which could help identify and protect the MD intraoperatively and decompress the pancreatic duct to reduce POPF.[3] But this method also has some disadvantages. Preoperative placement of a pancreatic duct stent is usually performed using an Endoscopic Retrograde Cholangiopancreatography (ERCP) approach, which could fail and increase the economic burden and hospital duration of the patient. Furthermore, it could lead to post-ERCP pancreatitis, subsequent pancreatic edema, and inflammation, which makes surgery more difficult.[4]

MDFAPE is a novel approach for PE and has several advantages over TPE. Firstly, the MD was first exposed, so it could be protected under direct vision. Secondly, reconfirmation of the integrity of the MD was performed if necessary to prevent POPF. Thirdly, this surgical approach ensured complete resection of the solid tumors and avoided R1 margins. Finally, after exposure of the MD, we could accurately suture the pancreatic tissue for hemostasis, without worrying about tying the MD.

This study indicated that with this approach, complete R0 resection of the tumors was achieved in all 21 cases ≤2 mm away from the MD in the MDFAPE group. The clinical POPF rate was significantly higher in the MDFAPE group (P <0.001), the reason might be that the MDFAPE procedure required dissection along the MD, which might cause damage to smaller, more invisible branch ducts that could not be ligated. However, higher clinical POPF did not lead to a higher incidence of severe postoperative complications (≥Grade III, P = 0.515), and most of the clinical POPF (12/14) only led to a longer drain removal time. The reason for the higher rate of laparoscopic surgery in the TPE group (P = 0.001) might be that MDFAPE is a novel surgical approach, which is still in the exploratory stage, and the surgical skills are not yet refined.

In conclusion, MDFAPE is feasible and safe for benign or low-grade malignant lesions ≤2 mm away from the MD in certain cases. Meanwhile, more cases and a longer study duration period are still needed to further verify the short- and long-term outcomes of MDFAPE.

Funding

This research was funded by the Key Research and Development Projects in Sichuan Province (No. 2023YFS0316), Key R&D project of Science and Technology Department of Sichuan Province (No. 2021YFS0107).

Conflicts of interest

None.

Supplementary Material

Xing Wang and Xiang Fu contributed equally to this work.

How to cite this article: Wang X, Fu X, Chen YH, Zhang H, Zheng ZJ, Zhong XF, Wang R, Liu XB, Tan CL. Main duct-first approach: A potential expansion of indications for pancreatic enucleation in benign and low-grade malignant lesions. Chin Med J 2024;137:2236–2238. doi: 10.1097/CM9.0000000000003285
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