Combined invagination and duct-to-mucosa techniques with modifications: a new method of pancreaticojejunal anastomosis

Bin Zhu, Li Geng, You-Gang Ma, Yong-Jie Zhang and Meng-Chao Wu

Shanghai, China

Combined invagination and duct-to-mucosa techniques with modifications: a new method of pancreaticojejunal anastomosis

Bin Zhu, Li Geng, You-Gang Ma, Yong-Jie Zhang and Meng-Chao Wu

Shanghai, China

BACKGROUND:Soft pancreatic texture and a small main pancreatic duct are thought to be the most significant risk factors for the occurrence of pancreatic fistula (PF), a common and serious complication after pancreaticoduodenectomy (PD). This is in part due to the technical difficulties of pancreaticojejunostomy (PJ) posed by a soft gland with a normal-sized duct. To deal with this problem, we developed a new anastomotic technique which combines the two most widely used techniques, namely, the invagination technique and the duct-to-mucosa technique, with a modification of the suture route and insertion of a temporary stent tube.

METHODS:Between January 2003 and December 2009, ninetytwo consecutive patients underwent PD in which the new PJ technique was used. Charts and follow-up data of these patients were reviewed for operative details, early postoperative events, and outcomes at 6 months after the operation. PF was defined by the International Study Group on Pancreatic Fistula (ISGPF) guidelines and graded (A, B or C) according to the clinical procedures and outcome.

RESULTS:In this group of 92 patients, there was only 1 early death from acute renal failure. PF was observed in 11 patients (12.0%), 8 in grade A, 1 in grade B, and 2 in grade C. For the 2 patients in grade C, PF was surgically managed. There were no early or late deaths attributable to PF. Six months after the operation, all of the patients were free of PJ-related symptoms except for 2, who were found to have steatorrhea.

CONCLUSIONS:Our modified technique is simple and safe in PD. Present data suggest that this technique produces excellent early and medium-term results.

(Hepatobiliary Pancreat Dis Int 2011; 10: 422-427)

pancreaticoduodenectomy; pancreaticojejunostomy; pancreatic fistula

Introduction

Despite recent advances in operative techniques and postoperative care, pancreatoenterostomic leakage is still a common and serious complication after pancreaticoduodenectomy (PD).[1-5]Many factors are associated with an increased incidence of this complication.[6-9]Among them, a soft pancreas with a small and thin pancreatic duct creates one of the technical hurdles to completion of the anastomosis, and is known to be a risk factor for major leakage.[10]Several methods have been advocated to reduce the occurrence of leakage, but the best technique is still a subject of debate.[11-18]

In this study, we report a new anastomotic technique which we developed for pancreaticojejunostomy (PJ) by combining the two most widely used techniques, namely, the invagination technique and the duct-to-mucosa technique, with a modification of the suture route and insertion of a temporary stent tube.

Methods

Patients

This review was conducted under a protocol approved by the Institutional Research Board of the Eastern Hepatobiliary Surgery Hospital with a waiver of individual patient consent (April 28, 2010).

From January 2003 to December 2009, we performed PD in 92 consecutive patients using the new PJ technique at our institution. There were 59 men and 33 women, with a mean age of 56.3±13.8 (range 18-75) years. Diagnoses were pancreatic head carcinoma (n=31), common bile duct carcinoma (25), adenocarcinoma of the major duodenal papilla (16), ampullary carcinoma(11), malignant pancreatic islet cell tumor (2), chronic pancreatitis (2), pancreatic head cystic carcinoma (1), pancreatic head cystadenoma (1), pancreatic head carcinoid (1), hamartoma of the major duodenal papilla (1), and descending duodenum inflammatory stenosis (1). During surgery, the diameter of the main pancreatic duct at the cut face measured <3 mm in 44 patients and ≥3 mm in 48.[6]As noted by the surgeon during the operation, the pancreatic texture was soft or normal in 41 patients, intermediate in 13, and hard in 38.[19]

Complications were graded according to Clavien's classification.[20]In accordance with the International Study Group on Pancreatic Fistula (ISGPF) guidelines, pancreatic fistula (PF) was diagnosed if amylase-rich fluid (i.e., drainage fluid with an amylase concentration more than 3 times of that in the serum) was collected by needle aspiration in intra-abdominal collection or from the intraoperatively placed drain on or after the third postoperative day.[21]PF was graded according to the clinical impact on the patient's hospital course (A, B, or C).[21]

All patients were evaluated for development of steatorrhea, diabetes, dilatation of the remnant pancreatic duct, and body weight gain 6 months after surgery.

Surgical technique for reconstruction

As Khan et al[22]reported, our reconstruction after the Whipple procedure was done with a modified Child method, performing the PJ to the end of an isolated Roux-en-Y limb bearing both the pancreatic and biliary anastomoses (Fig. 1).

Surgical technique for PJCutting the pancreas

Fig. 1. Isolated Roux-en-Y biliary and pancreatic anastomoses.

A suture was placed at the superior margin and the inferior margin of the planned pancreatic cut line, both for marking and for hemostasis. The pancreas was then cut with electrocautery (or a scalpel if the pancreatic duct was not significantly dilated). Active bleeding was controlled by 3-0 silk figure-of-eight sutures. The opening of the pancreatic duct on the cut face was noted. For this technique, approximately 2 cm of the cut end of the pancreatic remnant was mobilized off the splenic vein.

Preparing the isolated Roux-en-Y limb

The jejunum was cut and the cut end of the anal side was moved up retrocolically through the hole in the right side of the transverse mesocolon. Compression and distortion of the mesostenium were avoided. About 50-60 cm of the jejunal cut end formed a blind loop and an end-to-side or end-to-end anastomosis of the pancreas and jejunum was performed.

The new anastomotic technique

Anastomosis of the pancreatic remnant and the small bowel was performed in 2 ways, depending on the size of the pancreatic stump: an end-to-end technique was used if the pancreatic stump matched the jejunal lumen well and an end-to-side technique was used if there was a mismatch. In the latter, the proximal end of the jejunum and the cut end of the pancreas were brought alongside. On the antimesenteric border of the jejunum, 3 to 5 cm distal to the oversewn staple line, a large full-thickness jejunotomy was created using electrocautery. The size of the jejunotomy was matched with the pancreatic stump. Of note, the jejunotomy was in actuality not done until the posterior outer row of sutures was finished.

As in the classic invagination technique, the anastomosis began with a posterior outer row of 3-0 nonabsorbable mattress sutures, starting at the superior margin of the pancreas and extending to the inferior margin. These sutures were placed approximately 5 to 10 mm away from the edge of the pancreas, taking bites in the pancreatic parenchyma (but sparing the main pancreatic duct) and the seromuscular layer of the jejunum. After all sutures were placed, they were tied. Then the jejunum was opened with an electrocautery (Fig. 2A).

A 6-12 Fr stent tube was inserted into the main pancreatic duct and used as a guide for further suture placements. The inner posterior layer of sutures was then placed with 3-0 silk sutures in an interrupted fashion, starting from the superior edge of the anastomosis and extending to the inferior edge. For each stitch, the needle entered the pancreatic parenchyma from within the pancreatic duct lumen, exited from the cut face atthe exterior edge, and then entered the posterior wall of the jejunum (approximately 1-1.5 cm from the cut edge, which was equivalent to the distance between the entrance and the exit of the needle on the pancreatic cut face), passed through the seromuscular layer and ultimately emerged from the mucosa at the intestinal cut edge (Fig. 2B). About 5 to 7 sutures were usually needed for the inner posterior layer, depending on the size of the pancreatic remnant. After all the sutures in the inner posterior layer were placed, they were tied one by one. Specifically, one of the sutures was further tied over the stent tube for its fixation. Thus, the wall of the main pancreatic duct as well as large amounts of the pancreatic parenchyma, and all layers of the jejunal wall were sutured. Great caution was taken to prevent tearing of the pancreatic parenchyma and to adequately fix the pancreas and jejunum.

The sutures for the anastomosis of the inner anterior wall were placed in the same way as those for the posterior wall (Fig. 2C). After that, the anterior outer row of 3-0 nonabsorbable mattress sutures were placed, while completing the anastomosis. Particularly, a pair of horizontal mattress sutures were placed for reinforcement at the junction of the posterior half and the anterior half of the outer layer of sutures. Thus, the invagination of the pancreatic remnant into the lumen of the jejunum was accomplished as well as the mucosato-mucosa anastomosis of the pancreatic duct and the jejunum (Fig. 2D). For the end-to-end anastomosis, it was advisable to mobilize 1.5-2 cm of the cut end of the jejunum.

Fig. 2. Details of our PJ technique that combines the invagination technique and the duct-to-mucosa technique with modifications. A: The posterior outer row of interrupted sutures. B: Suture placement for the inner layer. For better demonstration, the stent tube inserted into the pancreatic duct as a guide (as shown in the inset) is omitted. C: View of the completed inner layer anastomosis. D: View of completed anastomosis of the inner and outer layers. The jejunum is transected to allow for an intra-lumen view. Note the jejunal folds formed around the opening of the pancreatic duct (inlet). P: pancreas; J: jejunum.

The stent tube in the pancreatic duct was introduced externally through the jejunal wall and the abdominal wall for external drainage of the pancreatic juice. Or, alternatively, it was cut short to about 10 cm at the jejunal end and left in the intestinal lumen for internal drainage.

Results

Postoperative complications are listed in Table 1. In this group of 92 patients, there was one death from acute renal failure on postoperative day 17, but this was not attributable to a PF. According to the definitions and grading system suggested by Bassi and colleagues,[21]PF occurred in 11 patients (12.0%, 11/92), of whom 8 were in grade A with no major clinical impact. One patient was in grade B and 2 in grade C (Table 2). Only the 2 patients in grade C (patients 1 and 2) were surgically managed by external drainage of bile and pancreatic juice. The patient in grade B (patient 3) underwent percutaneous drainage under the guidance of B-ultrasonography.

Of the 91 patients who were discharged from hospital, 86 were followed up for 6 months postoperatively. Seventeen patients had tumor recurrence causing 2 deaths. Two patients with grade C PF needed digestivetract reconstruction. In the remaining 67 patients, steatorrhea, diabetes, dilatation of the remnant pancreatic duct or body weight gain were determined. Only steatorrhea was found in 2 patients. No new onset of diabetes was found. Of the 62 patients who underwent a computed tomography or magnetic resonance imaging, none had anastomotic stenosis of PJ or pancreatic ductal dilatation.

Table 1. Postoperative complications (Clavien's classification)

Table 2. Details of grade B and C pancreatic fistula management

Discussion

PF is the major cause of postoperative morbidity and mortality after PD. The incidence of PF ranges between 5% and 30% according to the definition used.[23-25]Many risk factors for PF have been identified and the most significant ones are thought to be a soft pancreatic texture and a small pancreatic duct. To date, 3 prospective randomized trials have investigated the relationship between the technique of PJ and the incidence of PF.[17,26,27]However, consensus is not reached in their conclusions. It is still largely the surgeon's preference that determines the technique of choice, which most often is an invagination technique or a duct-to-mucosa technique. Technically, a PJ is easy to perform in patients with a dilated pancreatic duct and hardened pancreatic parenchyma. But, if the pancreas is normal, difficulty always exists in the anastomosis of the fragile parenchyma and the small pancreatic duct to the jejunum.[27]

For the PJ procedure, the invagination technique is chosen primarily for its relative simplicity and the flexibility that allows for either end-to-end or end-toside anastomosis. However, with this technique, the cut face of the pancreas is partially exposed to the intestinal lumen and subject to the erosion of digestive juice, which might lead to bleeding, tissue necrosis and often stenosis of the opening of the pancreatic duct. Furthermore, the invagination technique entails an inner layer of sutures that incorporate limited pancreatic tissues, which might be prone to tear in patients with a soft and fragile pancreatic texture. In contrast, the duct-to-mucosa technique is advantageous by covering the cut face of the pancreas with the jejunal serosa, hence preventing tissue necrosis and bleeding and rendering a superior pancreatic duct patency. But only end-to-side anastomosis can be performed with this technique and the operation can be quite difficult, particularly when a small pancreatic duct (<3 mm in diameter) is encountered. As discussed above, soft and fragile pancreatic tissue and small pancreatic duct can be problematic for both the invagination technique and the duct-to-mucosa technique, the former liable to parenchymal tearing and the latter liable to inaccurate suture placement.

To overcome the technical difficulties of performing a pancreaticoenterostomy with a soft pancreas, we developed a new anastomotic technique that combined the invagination technique and the duct-to-mucosa technique with a modified suture route and insertion of a temporary stent tube. The key points of our technique should be known. First, based on the invagination technique, we altered the suture route of the inner layer of the sutures, incorporating more pancreatic tissues and also part of the pancreatic duct wall and therefore reinforcing the sutures, preventing parenchymal tearing and making the anastomosis safer for a normal and soft pancreas. Second, we used a stent tube of appropriate diameter during the anastomosis. The stent tube actedas a guide to support the pancreatic duct lumen and prevented the duct from collapsing, which ensured adequate pancreatic duct exposure, accurate suture placement, and protection of the opposite wall from being inadvertently caught by needles.

The strength of our technique lies in its combination of the advantages and elimination of the disadvantages of the invagination and the duct-to-mucosa techniques. First, the sutures incorporated the pancreatic duct wall as well as half of the cut face of the pancreas, making it less likely to tear through the tissues in case of a soft and fragile pancreas. Second, modified from the invagination technique, our technique is also relatively simple and allows for both end-to-end and end-to-side anastomosis. Third, with our technique, the cut face of the pancreas is covered by the jejunal wall and a ductto-mucosa anastomosis can be accomplished either in an end-to-end or end-to-side manner, leading to less possibility of tissue necrosis, bleeding or stenosis of the opening of the pancreatic duct. Fourth, the stent tube facilitates the operation in case of a small pancreatic duct and helps maintain the patency of the anastomosis.

Theoretically, there might be concern with our technique about the mismatch of the diameter of the pancreatic duct and the size of the jejunal lumen or the jejunostomy. The mismatch might produce folds of jejunal wall around the opening of the pancreatic duct, leaving gaps upon the cut face of the pancreas that might give rise to pancreatic juice leakage. But, in our practice and also through experience gained from intestinal anastomosis, by spacing the stitches below 5 mm on the jejunal side, the gaps were minimized to a negligible degree. Moreover, the outer layer of invaginating sutures further reduced the possibility of pancreatic juice leakage. However, the jejunal folds formed around the opening of the pancreatic duct make it strongly advisable to leave the stent tube in place for prevention of anastomotic stenosis.

It is noteworthy that the inner layer sutures used for PJ anastomosis have evolved from nonabsorbable to absorbable materials.[28]The current trend in suture selection reflects the reasonable concern about stone formation in the anastomotic stoma. In our series, 3-0 silk sutures were used for the duct-to-mucosa component of the anastomosis. This was largely due to the influence of our long-standing surgical habit. Also, no complications were found that could be attributed to silk sutures in our experience so far. But in a larger patient population, we speculate that nonabsorbablesuture-related complications may occur and absorbable sutures may be superior.

Compared with the results in the literature,[1-5,25-27]the incidence of PF associated with our technique was low (12.0%, 11/92) and no PF-related deaths occurred in this group. This result shows that our technique is safe for PJ.

In summary, our modified technique is simple and safe in PD. Although more cases and longer followup are needed for better determination of its efficacy, the present data suggest that this technique produces excellent early and medium-term results and should be considered in the armamentarium of any surgeon who performs PD regularly.

Acknowledgement

We thank Dr. Hao Tang of Shanghai Changhai Hospital for his aid in the preparation of the manuscript.

Funding:This study was supported by a grant from the Natural Science Foundation of Shanghai (09ZR1400900).

Ethical approval:The modified technique was approved by the Ethics Committee of the Eastern Hepatobiliary Surgery Hospital in China (2002-007). Written informed consent was obtained from all patients or their surrogates before operation.

Contributors:ZB and GL contributed equally to this work. MYG proposed the study. ZB and GL wrote the first draft. ZB, GL and MYG analyzed the data. ZYJ and WMC contributed to the design and checked the draft. All authors contributed to the design and interpretation of the study and to further drafts. MYG is the guarantor.

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.

1 Cameron JL, Riall TS, Coleman J, Belcher KA. One thousand consecutive pancreaticoduodenectomies. Ann Surg 2006;244: 10-15.

2 Yeo CJ, Cameron JL, Sohn TA, Lillemoe KD, Pitt HA, Talamini MA, et al. Six hundred fifty consecutive pancreatico duodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997;226:248-260.

3 Aranha GV, Aaron JM, Shoup M, Pickleman J. Current management of pancreatic fistula after pancreaticoduodenectomy. Surgery 2006;140:561-589.

4 Grobmyer SR, Pieracci FM, Allen PJ, Brennan MF, Jaques DP. Defining morbidity after pancreaticoduodenectomy: use of a prospective complication grading system. J Am Coll Surg 2007;204:356-364.

5 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.

6 Pratt WB, Callery MP, Vollmer CM Jr. Risk prediction for development of pancreatic fistula using the ISGPFclassification scheme. World J Surg 2008;32:419-428.

7 Muscari F, Suc B, Kirzin S, Hay JM, Fourtanier G, Fingerhut A, et al. Risk factors for mortality and intra-abdominal complications after pancreatoduodenectomy: multivariate analysis in 300 patients. Surgery 2006;139:591-598.

8 Lin JW, Cameron JL, Yeo CJ, Riall TS, Lillemoe KD. Risk factors and outcomes in postpancreaticoduodenectomy pancreaticocutaneous fistula. J Gastrointest Surg 2004;8:951-959.

9 Gaujoux S, Cortes A, Couvelard A, Noullet S, Clavel L, Rebours V, et al. Fatty pancreas and increased body mass index are risk factors of pancreatic fistula after pancreaticoduodenectomy. Surgery 2010;148:15-23.

10 DeOliveira ML, Winter JM, Schafer M, Cunningham SC, Cameron JL, Yeo CJ, et al. Assessment of complications after pancreatic surgery: A novel grading system applied to 633 patients undergoing pancreaticoduodenectomy. Ann Surg 2006;244:931-939.

11 Connor S, Alexakis N, Garden OJ, Leandros E, Bramis J, Wigmore SJ. Meta-analysis of the value of somatostatin and its analogues in reducing complications associated with pancreatic surgery. Br J Surg 2005;92:1059-1067.

12 Lee SE, Ahn YJ, Jang JY, Kim SW. Prospective randomized pilot trial comparing closed suction drainage and gravity drainage of the pancreatic duct in pancreaticojejunostomy. J Hepatobiliary Pancreat Surg 2009;16:837-843.

13 Grobmyer SR, Kooby D, Blumgart LH, Hochwald SN. Novel pancreaticojejunostomy with a low rate of anastomotic failure-related complications. J Am Coll Surg 2010;210:54-59.

14 Sugiyama M, Suzuki Y, Abe N, Ueki H, Masaki T, Mori T, et al. Pancreatic duct holder for facilitating duct-to-mucosa pancreatojejunostomy after pancreatoduodenectomy. Am J Surg 2009;197:e18-20.

15 Kakita A, Yoshida M, Takahashi T. History of pancreaticojejunostomy in pancreaticoduodenectomy: development of a more reliable anastomosis technique. J Hepatobiliary Pancreat Surg 2001;8:230-237.

16 Payne RF, Pain JA. Duct-to-mucosa pancreaticogastrostomy is a safe anastomosis following pancreaticoduodenectomy. Br J Surg 2006;93:73-77.

17 Peng SY, Wang JW, Lau WY, Cai XJ, Mou YP, Liu YB, et al. Conventional versus binding pancreaticojejunostomy after pancreaticoduodenectomy: a prospective randomized trial. Ann Surg 2007;245:692-698.

18 Kimura W. Pancreaticojejunal anastomosis, using a stent tube, in pancreaticoduodenectomy. J Hepatobiliary Pancreat Surg 2009;16:305-309.

19 Yeo CJ, Cameron JL, Lillemoe KD, Sauter PK, Coleman J, Sohn TA, et al. Does prophylactic octreotide decrease the rates of pancreatic fistula and other complications after pancreaticoduodenectomy? Results of a prospective randomized placebo-controlled trial. Ann Surg 2000;232:419-429.

20 Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205-213.

21 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.

22 Khan AW, Agarwal AK, Davidson BR. Isolated Roux Loop duct-to-mucosa pancreaticojejunostomy avoids pancreatic leaks in pancreaticoduodenectomy. Dig Surg 2002;19:199-204.

23 Bassi C, Butturini G, Molinari E, Mascetta G, Salvia R, Falconi M, et al. Pancreatic fistula rate after pancreatic resection. The importance of definitions. Dig Surg 2004;21: 54-59.

24 Butturini G, Daskalaki D, Molinari E, Scopelliti F, Casarotto A, Bassi C. Pancreatic fistula: definition and current problems. J Hepatobiliary Pancreat Surg 2008;15:247-251.

25 Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience. J Gastrointest Surg 2006;10:1199-1211.

26 Bassi C, Falconi M, Molinari E, Mantovani W, Butturini G, Gumbs AA, et al. Duct-to-mucosa versus end-to-side pancreaticojejunostomy reconstruction after pancreaticoduodenectomy: results of a prospective randomized trial. Surgery 2003;134:766-771.

27 Berger AC, Howard TJ, Kennedy EP, Sauter PK, Bower-Cherry M, Dutkevitch S, et al. Does type of pancreaticojejunostomy after pancreaticoduodenectomy decrease rate of pancreatic fistula? A randomized, prospective, dual-institution trial. J Am Coll Surg 2009;208:738-749.

28 Shukla PJ, Barreto SG, Fingerhut A, Bassi C, Büchler MW, Dervenis C, et al. Toward improving uniformity and standardization in the reporting of pancreatic anastomoses: a new classification system by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 2010;147:144-153.

Received March 21, 2011

Accepted after revision June 9, 2011

Author Affiliations: Second Department of Biliary Surgery (Zhu B, Ma YG and Zhang YJ) and Department of Special Treatment (Gengland Wu MC), Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai 200438, China

You-Gang Ma, MD, Second Department of Biliary Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, 225 Changhai Road, Shanghai 200438, China (Tel: 86-21-81875272; Fax: 86-21-81875093; Email: yougangma@sina.cn)

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