Ligamentum teres hepatis patch enhances the healing of pancreatic fistula after distal pancreatectomy
Chun-Tao Wu, Wen-Yan Xu, Liang Liu, Jiang Long, Jin Xu, Quan-Xing Ni, Chen Liu and Xian-Jun Yu
Shanghai, China
Author Affiliations: Pancreatic Cancer Institute, Fudan University; Department of Pancreatic and Hepatobiliary Surgery, Fudan University Shanghai Cancer Center; Department of Oncology, Shanghai Medical College, Fudan University, Shanghai 200032, China (Wu CT, Xu WY, Liu L, Long J, Xu J, Ni QX, Liu C and Yu XJ)
Corresponding Author: Xian-Jun Yu, MD, PhD, Pancreatic Cancer Institute, Fudan University; Department of Pancreatic and Hepatobiliary Surgery, Fudan University, Shanghai Cancer Center; Shanghai 200032, China (Tel: 86-21-64175590ext1307; Fax: 86-21-64031446; Email: yuxianjun88@hotmail.com)
© 2013, Hepatobiliary Pancreat Dis Int. All rights reserved.
doi: 10.1016/S1499-3872(13)60102-2
Contributors: LC and YXJ proposed the study. WCT and XWY performed research and wrote the first draft. WCT collected and analyzed the data. WCT, XWY and LC contributed equally to this work. All authors contributed to the design and interpretation of the study and to further drafts. YXJ is the guarantor.
Funding: This work was supported by grants from the National Natural Science Foundation of China (81001058, 81172276 and 81172005), the National Natural Science Foundation of Shanghai (11ZR1407000), and PhD Programs Foundation of Ministry of Education of China (20110071120096).
Ethical approval: The study was approved by the Fudan University Cancer Center Research Ethics Committee. Informed consent was obtained according to its regulations.
Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.
ABSTRACT: Pancreatic fistula is one of the most common complications after the distal pancreatectomy. Many methods have been tried to solve the problem, but no one is optimal, especially for the soft pancreatic stump cases. This study used ligamentum teres hepatis as a patch to cover the pancreatic stump. Between October 2010 and December 2012, seventy-seven patients who had undergone distal pancreatectomy with a soft pancreatic stump were divided into two groups: group A (n=39, patients received conventional ligated main pancreatic duct method) and group B (n=38, patients underwent a coverage procedure). Patients in group A had a longer recovery from postoperative pancreatic fistula than those in group B (16.4±3.5 vs 10.8±1.6 days, P<0.05). The coverage procedure with ligamentum teres hepatis is a safe, effective and convenient method for patients with a soft pancreas remnant during distal pancreatectomy.
(Hepatobiliary Pancreat Dis Int 2013;12:651-655)
KEY WORDS: distal pancreatectomy; pancreatic fistula; complications
Introduction
Pancreatic fistula was one of the most common complications of the distal pancreatectomy and was also the main cause of the other postoperative complications such as postoperative hemorrhage, intra-abdominal abscess, sepsis and delayed gastric emptying (DGE).[1,2] The overall incidence of the pancreatic fistula in patients after distal resection of the pancreas varied from 10% to 30%.[3-6] In an attempt to reduce the incidence of the pancreatic fistula, various surgical techniques were explored,[7-10] such as management of the pancreatic parenchyma (cutting by sharp blades, electrotome or ultrasonic dissector), and the closure of the pancreas remnant (ligation of the main pancreatic duct, sew up the remnant by hand, anastomosis between the remnant and the jejunum or usage of the biological glue). However, there was no omnipotent method for all the patients, especially in patients with soft pancreas remnant. Covering the pancreatic remnant with a seromuscular patch was a fast, technically feasible method which could decrease the rate of postoperative pancreatic fistula (POPF), but the method increased the incidence of DGE, which impeded its extensive application.[11,12] Clinically, we modified the closure method that the ligamentum teres hepatis was used as a serosa patch, rather than a seromuscular patch, to cover the pancreas remnant following ligation of the main pancreatic duct. Our approach exhibited some advantages compared with conventional main pancreatic ligation method in the cases of normal soft pancreatic stump.
Methods
Patients
Between October 2010 and December 2012, seventy-seven patients who had undergone distal pancreatectomy were included in the retrospective study. All patients had lesions located in the body or tail of the pancreas, consisting of 37 malignant tumors, 20 benign tumors, 15 borderline tumors, and 5 inflammatory lesions. All of them were soft pancreas cases which defined as a pancreas with normal exocrine and endocrine functions, with a diameter of the main pancreatic duct <3.0 mm in the head and absence of fibrosis or pancreatitis in postoperative pathologic specimens.[13-15] All of the resection margins were located at the neck of the pancreas. The 77 patients were divided into two groups, 39 patients in group A who underwent direct ligation of the main pancreatic duct and an inverting closure of the pancreas remnant, while the other 38 patients in group B were subjected to a mesh-like ligamentum teres hepatis to cover the pancreas remnant after ligation of the main pancreatic duct and the inverting closure of the pancreas remnant. The operations for the two groups were performed by two surgeons. Prophylactic octreotide was not used in all patients. Drain amylase was measured on the postoperative day 3, 5, and 7 to exclude pancreatic fistula and to estimate the severity of pancreatic fistula; CT scans were performed within 1 week if necessary to rule out peritoneal effusion, abscess, or leakage. POPF, postpancreatectomy hemorrhage (PPH), and DGE were defined and classified according to the International Study Group of Pancreatic Surgery (ISGPS).[16-20] The duration of POPF was calculated until no measurable volume of drainage fluid.
Surgical techniques
Isolation of the pancreatic parenchyma at the neck of the pancreas was performed by an electrocauter. In group A, after distal pancreatectomy with or without splenectomy, the main pancreatic duct on the cut surface was identified and isolated by a surgical knife, then the duct was directly ligated and the pancreatic stump was sutured interruptedly using 4-0 absorbable stitches (Fig. 1). In group B, the same procedure was performed to manage pancreatic stump as in group A. Subsequently, 1) the ligamentum teres hepatis with blood supply was detached from the abdominal wall from the umbilicus for an adequate length of about 5-7 cm; 2) the fat tissue attached to the ligament was removed; 3) the ligament was sutured to the serosa of the pancreatic stump with 4-0 absorbable sutures. The ligament was in a tension-free condition after the coverage procedure had completed (Fig. 2). Finally, two drain tubes were placed around the pancreatic remnant.
Postoperative management
The drain amylase level was measured at the third, fifth, seventh day after the operation, and pancreatic fistula was excluded if the drain amylase level was lower than 3 times of the serum amylase level on postoperative day 3. The drain tubes were removed within 1 week. Fistulas were graded according to the definition of International Study Group of Pancreatic Fistula (ISGPF). For the cases of POPF grade A, the timing to withdraw the drain tubes was delayed; the drain tube was removed slowly according to the drain amylase level and volume. In the cases of POPF grade B, the drain tubes were usually maintained in situ for at least 3 weeks. If patients suffered from a peritoneal effusion or abscess, the drain tubes were repositioned by an interventional drainage procedure under the guidance of CT or ultrasound.
Statistical analysis
Comparisons between the two groups were done using the Chi-square test or Fisher's exact test, and the averages were compared using Student's t test. P<0.05 was considered statistically significant. Numeric data were expressed as mean±standard deviation.
Results
In the 77 patients with normal soft pancreatic remnant, 39 (group A) underwent a direct ligation of the main pancreatic duct followed by an inverting closure of the pancreas remnant, while another 38 patients (group B) were treated by a mesh-like ligamentum teres hepatis to cover the pancreas remnant. There were no statistical differences between the two groups in terms of gender, age, BMI, entities of diseases, operation time, and splenectomy. The size of the main pancreatic duct for the two groups was almost the same (2.2±0.2 vs 2.4±0.2 mm, P>0.05) (Table 1).
Postoperative complications (Table 2) included POPF, postoperative hemorrhage, intra-abdominal abscesses, sepsis, and DGE. The overall POPF rate in group A was 30.8% (12/39), compared with 26.3% (10/38) in group B (P>0.05). Grade of POPF showed no difference between the two groups (grade A/B/C, 10/2/0 vs 9/1/0, respectively, P>0.05). POPF in group A was a statistically longer than that in group B (16.4±3.5 vs 10.8±1.6 days, P<0.05). All of the POPF grade A cases were fed orally with favorable clinical results. Two patients with POPF grade B in group A was treated conservatively by initial drainage without additional intervention. Table 3 shows the trend of the drain amylase at the third, fifth and seventh day after operation for all patients. There was no statistical differences between the two groups for the third and fifth day (P>0.05). At day 7, four patients in group A had the amylase level in drainage decreased to a normal level, whereas 8 patients in group B showed a significant difference between the two groups (P<0.05). Octreotide was not applied in this series. However, if there was evidence of remnant pancreatitis, octreotide would be used until the serum amylase returned to normal.
The operation time for the pancreatic stump in group A was shorter than that in group B (8.1±1.7 vs 19.8±3.2 min, P<0.05), but there was no significant difference in the operation time between the two groups (228.7±84.3 vs 231.7±55.9 min, P>0.05).
Discussion
At present, pancreatic fistula after distal pancreatectomy remains a problem although various methods have been used to reduce its incidence.[21, 22] There was no difference in POPF between the open and laparoscopic procedures, and no unequivocal evidence showed that the methods of transection of the pancreatic parenchyma, including ordinary blade, electrotome, ultrasonic dissector, bipolar electrotome and straight closure contributed to a raised POPF rate.[11] Kleeff et al[5] reported that stapler closure of the pancreatic remnant is associated with a significantly higher fistula rate. The utilization of the mesh to cover the pancreas remnant and some other managements including the pancreas remnant to jejunum anastomosis, closure of the stump by biological glue, are still controversial, and no obvious effect on the reduction of the POPF has been reported.[8, 10]
The texture of the pancreas remnant was another crucial issue involving the occurrence of the pancreatic fistula, a hard pancreas remnant indicates that the patient would have suffered from chronic pancreatitis or other chronic inflammations previously, which lead to exocrine pancreatic insufficiency and a falling pancreatic juice output.[23] Meanwhile, it is comparatively easy to treat a hard pancreas remnant with less pancreatic fistula developed after operation. In the normal soft pancreas cases, however, there are various tiny branches of the pancreatic duct accompanied with the main pancreatic duct on the cutting surface of the pancreatic stump. Even if the main pancreatic duct has been ligated, some missed tiny branches of the pancreatic duct might secrete the pancreatic juice into the abdominal cavity, resulting in pancreatic fistula, infection, abscess, or hemorrhage.
In our patients, the incidence of POPF was relatively high in patients with normal soft pancreas tissue. We used ligamentum teres hepatis as a patch to cover the stump to improve the POPF after distal pancreatectomy with a soft pancreatic stump. First, after direct ligation of the main pancreatic duct and closure of the pancreatic parenchyma, the coverage of the pancreatic stump with ligamentum teres hepatis could effectively reduce pancreatic juice leakage from the injured tiny branches of the pancreatic duct. Second, we specially reserved blood supply of the ligamentum teres hepatis, which might provide a favorable condition after ligament coverage to promote the healing of the pancreatic remnant and, therefore, to enhance the recovery from POPF. In this study, there was no difference in the incidence rate of POPF, but the length of POPF was significantly shorter in group B than that in group A. The finding indicates that the novel method promotes the healing of pancreatic fistula, and improves the outcomes in case of POPF to some extent.
We spent several minutes on treating and covering the ligamentum teres hepatis, but this did not significantly increase the operation time. Furthermore, several studies demonstrated that the covering of pancreatic remnant with a seromuscular patch would not be recommended because of a high rate of DGE.[24] The patients in group B did not experience a DGE. We did not use the gastric or intestinal wall as a patch, which might explain the lower incidence of DGE.
In summary, ligamentum teres hepatis patch is technically feasible and safe for the management of a soft pancreas remnant. This new procedure shortens the length of POPF. A future prospectively randomized trial is needed to validate the benefit of this technique.
References
1 Andrén-Sandberg A, Wagner M, Tihanyi T, Löfgren P, Friess H. Technical aspects of left-sided pancreatic resection for cancer. Dig Surg 1999;16:305-312. PMID: 10449975
2 Knaebel HP, Diener MK, Wente MN, Büchler MW, Seiler CM. Systematic review and meta-analysis of technique for closure of the pancreatic remnant after distal pancreatectomy. Br J Surg 2005;92:539-546. PMID: 15852419
3 Oláh A, Issekutz A, Belágyi T, Hajdú N, Romics L Jr. Randomized clinical trial of techniques for closure of the pancreatic remnant following distal pancreatectomy. Br J Surg 2009;96:602-607. PMID: 19434697
4 Sledzianowski JF, Duffas JP, Muscari F, Suc B, Fourtanier F. Risk factors for mortality and intra-abdominal morbidity after distal pancreatectomy. Surgery 2005;137:180-185. PMID: 15674199
5 Kleeff J, Diener MK, Z'graggen K, Hinz U, Wagner M, Bachmann J, et al. Distal pancreatectomy: risk factors for surgical failure in 302 consecutive cases. Ann Surg 2007;245:573-582. PMID: 17414606
6 Lillemoe KD, Kaushal S, Cameron JL, Sohn TA, Pitt HA, Yeo CJ. Distal pancreatectomy: indications and outcomes in 235 patients. Ann Surg 1999;229:693-700. PMID: 10235528
7 Ohwada S, Ogawa T, Tanahashi Y, Nakamura S, Takeyoshi I, Ohya T, et al. Fibrin glue sandwich prevents pancreatic fistula following distal pancreatectomy. World J Surg 1998;22:494- 498. PMID: 12555295
8 Hassenpflug M, Hartwig W, Strobel O, Hinz U, Hackert T, Fritz S, et al. Decrease in clinically relevant pancreatic fistula by coverage of the pancreatic remnant after distal pancreatectomy. Surgery 2012;152:S164-171. PMID: 22819173
9 Hackert T, Büchler MW. Remnant closure after distal pancreatectomy: current state and future perspectives. Surgeon 2012;10:95-101. PMID: 22113052
10 Wagner M, Gloor B, Ambühl M, Worni M, Lutz JA, Angst E, et al. Roux-en-Y drainage of the pancreatic stump decreases pancreatic fistula after distal pancreatic resection. J Gastrointest Surg 2007;11:303-308. PMID: 17458602
11 Bilimoria MM, Cormier JN, Mun Y, Lee JE, Evans DB, Pisters PW. Pancreatic leak after left pancreatectomy is reduced following main pancreatic duct ligation. Br J Surg 2003;90:190-196. PMID: 12555295
12 Pannegeon V, Pessaux P, Sauvanet A, Vullierme MP, Kianmanesh R, Belghiti J. Pancreatic fistula after distal pancreatectomy: predictive risk factors and value of conservative treatment. Arch Surg 2006;141:1071-1076. PMID: 17116799
13 Mariani A. Is secretin magnetic resonance cholangio-pancreatography an effective guide for a diagnostic and/or therapeutic flow-chart in acute recurrent pancreatitis? JOP 2001;2:414-421. PMID: 11880701
14 Shinchi H, Takao S, Maemura K, Fukukura Y, Noma H, Matsuo Y, et al. Value of magnetic resonance cholangiopancreatography with secretin stimulation in the evaluation of pancreatic exocrine function after pancreaticogastrostomy. J Hepatobiliary Pancreat Surg 2004;11:50-55. PMID: 15754047
15 Mortelé KJ, Rocha TC, Streeter JL, Taylor AJ. Multimodality imaging of pancreatic and biliary congenital anomalies. Radiographics 2006;26:715-731. PMID: 16702450
16 Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, et al. Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 2005;138:8-13. PMID: 16003309
17 Reid-Lombardo KM, Farnell MB, Crippa S, Barnett M, Maupin G, Bassi C, et al. Pancreatic anastomotic leakage after pancreaticoduodenectomy in 1507 patients: a report from the Pancreatic Anastomotic Leak Study Group. J Gastrointest Surg 2007;11:1451-1459. PMID: 17710506
18 Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, et al. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 2007;142:20-25. PMID: 17629996
19 Pratt WB, Maithel SK, Vanounou T, Huang ZS, Callery MP, Vollmer CM Jr. Clinical and economic validation of the International Study Group of Pancreatic Fistula (ISGPF) classification scheme. Ann Surg 2007;245:443-451. PMID: 17435552
20 Yekebas EF, Wolfram L, Cataldegirmen G, Habermann CR, Bogoevski D, Koenig AM, et al. Postpancreatectomy hemorrhage: diagnosis and treatment: an analysis in 1669 consecutive pancreatic resections. Ann Surg 2007;246:269-280. PMID: 17667506
21 Balcom JH 4th, Rattner DW, Warshaw AL, Chang Y, Fernandez-del Castillo C. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization. Arch Surg 2001;136:391-398. PMID: 11296108
22 Liu L, Xu HX, Wang WQ, Wu CT, Chen T, Qin Y, et al. Cavin-1 is essential for the tumor-promoting effect of caveolin-1 and enhances its prognostic potency in pancreatic cancer. Oncogene 2013 Jun 17. PMID: 23770857
23 Tran TC, van 't Hof G, Kazemier G, Hop WC, Pek C, van Toorenenbergen AW, et al. Pancreatic fibrosis correlates with exocrine pancreatic insufficiency after pancreatoduodenectomy. Dig Surg 2008;25:311-318. PMID: 18818498
24 Tani M, Terasawa H, Kawai M, Ina S, Hirono S, Uchiyama K, et al. Improvement of delayed gastric emptying in pylorus-preserving pancreaticoduodenectomy: results of a prospective, randomized, controlled trial. Ann Surg 2006;243:316-320. PMID: 16495694
Received April 1, 2013
Accepted after revision October 25, 2013 |