A simple pancreaticojejunostomy technique for hard pancreases using only two transpancreatic sutures with buttresses: a comparison with the previous pancreaticogastrostomy and dunking methods

Pancreaticoenteric anastomosis is one of the most important stages of pancreaticoduodenectomy (PD) procedures and often determines the overall outcomes of the surgery. It is quite different from other PD anastomoses, such as choledochojejunostomy, gastrojejunostomy, or duodenojejunostomy, for several reasons. First, the texture of the pancreas is commonly fragile, and this property creates some difficulties avoiding pancreatic laceration during suturing and might lead to pancreatic leakage. Second, the pancreas is fixed to the retroperitoneum, whereas the bowel is freely movable; therefore, pancreaticoenteric anastomosis might be less secure and easier to disrupt than other anastomoses between hollow visceral organs. Third, the dissection plane is usually near major vascular structures, such as the superior mesenteric artery, superior mesenteric vein (SMV), or the portal vein, and also adjacent to various organs, such as the stomach or duodenum, which makes performing the anastomosis more difficult.

Pancreases with a hard texture are thought to have a very low risk of postoperative pancreatic fistula (POPF), which results from anastomotic disruption. This complication is caused by the obstruction of the pancreatic duct by tissue fibrosis, which is one of the characteristics of hard pancreases. Moreover, the tissue strength without distortion or shattering against the shear stress of the needle (suture-holding capacity, SHC) is usually increased in hard pancreas cases, which is helpful for reducing the risk of POPF [1]. Therefore, improvements in technical complexity or difficulty have begun to emerge as a key aspect of pancreaticoenteric anastomosis rather than the type of anastomosis, especially for hard pancreas cases, which have a low risk of POPF.

In our institution, the authors previously proposed pancreaticogastrostomy (PG) using two transpancreatic sutures with buttresses (PGt) in 2010 [2], and we have tried to modify and develop another method to establish the safety and simplicity of pancreaticoenteric anastomosis, especially for hard pancreases. In this study, we introduced a novel technique, the pancreaticojejunostomy (PJ), which uses only two transpancreatic sutures with buttresses (PJt), and compared the surgical outcomes with the conventional dunking method (Du) and the previously described PGt method particularly for hard pancreases.

From March 2006 to March 2015, 231 patients with periampullary lesions underwent PD. All surgical procedures were performed by three specialized pancreas surgeons at our institution. Conventional end-to-end PJ (dunking method) has been the most common PD method performed by the three surgeons; however, surgeon Hong introduced the PGt method in May 2010. Using this method, the anastomosis is completed with two transpancreatic sutures with buttresses on both the upper and lower edges of the implanted pancreas into the stomach through the retracted anterior gastrostomy (Fig. 1) [2], and this technique has been consecutively applied in pancreaticoenteric anastomoses after PD by surgeon Hong In January 2013, the PJt method, which is a modification of the previous PGt method, was developed, and it has been performed only in hard pancreas cases. The hardness of the pancreas is estimated by the surgeon during the operation and is also more objectively based on a durometer measurement of the pancreas hardness using the same method described in previous reports (Fig. 2) [3, 4]. (We considered the pancreas hard when the durometer level was greater than 40 shore units, as described in a previous report.)

Fig. 1
A schematic diagram of pancreaticogastrostomy using two transpancreatic sutures with buttresses through a gastrostomy made in the anterior wall of stomach.

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Fig. 2
The hardness of the pancreas has been estimated based on the surgeon's judgment during the operation and more objectively using a durometer to measure the hardness of the pancreas.

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Data for all recruited cases were retrospectively reviewed and compared according to the types of pancreaticoenteric anastomosis. Because the PJt has been applied only in hard pancreas cases, in this study, we only enrolled cases in which the conventional Du or PGt were performed with hard pancreases. Among the cases, the patients who underwent any concurrent operation, such as hepatectomy or colectomy, were excluded, and some cases that involved pancreaticoenteric anastomoses, such as duct-to-mucosa PJ or binding PJ, were also excluded from this study. As a result, a total of 101 cases were included and categorized into three groups according to the type of pancreaticoenteric anastomosis: the Du group was performed on 30 patients, the PGt method (the PGt group) was performed on 31 patients, and the PJt method (the PJt group) was performed on 40 patients. All medical data were prospectively collected, including demographics (age, sex, body mass index, pathology, American Society of Anesthesiologists class, tumor characteristics), operative results (overall operative time, pancreaticoenteric anastomosis time, estimated blood loss, intraoperative transfusion) and postoperative outcomes (length of postoperative hospital stay, the start of soft diet, postoperative complications, and mortality).

Surgical technique

In the Du group, end-to-end dunking anastomosis was performed as described in the report by Batignani et al. [5]. In the PGt group, PG using two transpancreatic sutures with buttresses was performed as described in a previously published report [2]. In the PJt group, PJ using two transpancreatic sutures with buttresses was performed as described in the next paragraph. After the pancreaticoenteric anastomosis, end-to-side choledocojejunostomy and end-to-side gastrojejunostomy or duodenojejunostomy were performed to establish the continuity of the digestive tract. After completing the reconstruction, we used three closed-suction drains; one was located near the hepaticojejunostomy, and the other two drains were placed around the pancreaticoenterostomy site. Schematic diagrams of the PGt and PJt procedures after the completion of reconstruction are shown in Fig. 3.

Fig. 3
Schematic diagrams of pancreaticogastrostomy using two transpancreatic sutures with buttresses (A) and pancreaticojejunostomy using two transpancreatic sutures with buttresses (B) after the completion of the reconstruction.

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PJ using two transpancreatic sutures with buttresses

After the resection of the pancreas head and duodenum was completed and the specimen was retrieved, approximately 3–4 cm of the length of the pancreas remnant stump was dissected away from the splenic vein and retroperitoneal attachments. Small vessel branches that were located between the pancreas and the SMV or splenic vein were dissected with ultrasound scissors. The location of the main pancreatic duct was identified with a probe, and then, a short plastic stent was inserted at least 4 cm into the duct to avoid the compression of the duct during the ligation of the transpancreatic sutures and to prevent accidental suturing of this duct during the pancreaticoenteric anastomosis. Approximately 3 cm of the length of the stent was left on the cut surface, and a suture was applied to fix the stent to the duct. Two stay sutures on both corners of the pancreas stump were placed to provide traction for the pancreas stump into the jejunal lumen. After preparing the pancreas stump, at least 2 cm of the mucosal layer of the jejunum loop from the cut edge was cauterized with an Argon beam to prevent mucosal secretions. A small hole was made in the jejunum on the antimesenteric side, where the hepaticojejunostomy would be performed, and a Kelly clamp was inserted into the hole to grasp the stay sutures on the pancreas. The operator gently pulled the two stay sutures with the Kelly clamp, and then, the pancreatic stump was brought into the jejunum approximately 3–4 cm and implanted. Next, two transpancreatic sutures with buttresses were placed on both the upper and lower borders of the implanted pancreas through the jejunal limb that covered the pancreas (Fig. 4). This suturing required a pair of 2-0 monofilament polypropylene threads with the specified straight needle at each end (2-0 Prolene, Ethicon Inc., Somerville, NJ, USA) and four buttresses (TFE Polymer Pledget, Ethicon Inc.), which is similar to the PGt method except for the type of threads used (PGt uses 4-0 monofilament polypropylene threads with a straightened needle). First, the suture was passed directly from the anterior surface of the covered jejunal limb, and then, it penetrated the full thickness of the implanted pancreas at a level 2 cm below the cut surface, from the ventral surface to the dorsal surface; next, it passed through the posterior surface of the covered jejunal limb. After this step, the buttresses were inserted through each needle, and the anastomosis was completed with a knot that included the entire jejunal wall and the implanted pancreas. In this method, we did not place any additional reinforcement sutures on the anastomosis line.

Fig. 4
Operative view (A, B) and schematic diagram (C) of pancreaticojejunostomy using two transpancreatic sutures with buttresses.

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Hard pancreases are generally accepted as having a low risk of POPF due to the following characteristics. First, the fibrotic changes in the tissue, which are a common finding in hard pancreases, obstruct the minor ducts at the cut-surface of the pancreas, and this could help reduce POPF by blocking the secretions from these minor ducts. Second, the firm nature of the pancreas helps to increase the SHC of the pancreatic tissue itself, and this prevents parenchymal tearing by the suture or tying during the anastomosis. These unique characteristics of hard pancreases help surgeons reduce the chance of POPF and also reduce the worry over choosing the type of anastomosis, whether the conventional duct-to-mucosa method, invagination PJ or even PG. Instead, the technical ease and feasibility of the anastomosis is emphasized in the case of hard pancreases. The difficulty of handling the anastomosis could result in technical errors, affect the stability of the anastomosis or even worsen the stress on the operator. At our institution, surgeon Hong has performed PJt for pancreaticoenteric anastomosis, which is a modification of the PGt for hard pancreases, since January 2013, after ensuring the safety and feasibility of the method through animal experiments using dogs.

Recently, several randomized controlled trials were published describing the improved safety of PG over PJ [12, 13], and we also agree that the PG could be more effective at reducing the risk of POPF compared to PJ. Nevertheless, we have selectively performed PJt in hard-textured pancreases for several reasons. First, with PG anastomosis, gastric acid could neutralize the pancreatic enzymes that cause the increased deterioration of digestive function after surgery. Rault et al. [14] reported that PJ produced better pancreatic exocrine function than PG after PD. Lemaire et al. [15] also reported that most patients developed pancreas exocrine insufficiency after PD with PG. We expect that the PJt method could theoretically be more beneficial for preserving the exocrine function of the pancreas after surgery compared with the PGt method.

Second, the ease and simplicity of the PJt technique is a leading cause of changing anastomosis to PJt. PJt does not require suturing of the walls of tiny pancreatic ducts as in the conventional duct-to-mucosa method. Only two pancreas-penetrating sutures are required to complete the anastomosis without additional reinforcement sutures, and it is a quite small number of sutures compared with other previous techniques. Ohigashi et al. [16] also used straight needles with a penetrating suture in a U-like fashion; however, this procedure requires at least 4 to 8 pancreas sutures. The conveniences of our technique could help shorten the pancreaticoenteric anastomosis time and overall operation time. The shortening of the operation time could also be expected to reduce the physiologic stress on the patient, and it might ultimately help to speed up the recovery process.

Comparing the two similar techniques using transpancreatic sutures, PGt and PJt, the anastomosis time was shorter in PJt than in PGt. In PGt, the anterior gastrotomy as well as the posterior gastrotomy are needed to perform the anastomosis under direct vision, and the gastrotomy site has to be closed again. Moreover, the sufficient mobilization of the pancreas stump from the SMV or the retroperitoneum is a very important step in both PGt and PJt because the stability of the anastomosis can be achieved through the deep invagination of the pancreas into the stomach or jejunum. In the PGt anastomosis, the pancreas stump should be mobilized more upward for invaginating it securely into the posterior wall of the stomach, and this usually requires a longer length of pancreas mobilization than that needed with the PJt. The posterior wall of the stomach is not freely movable for displacement during the PG, and therefore, more sufficient mobilization of the pancreas stump without tension is needed despite the prolonged operation time. In contrast, the jejunum is more free to move, and it is more favorable for completing the anastomosis.

The incidence of grades B and C POPF in the groups using transpancreatic sutures (groups PGt and PJt) was zero, although these results were limited to hard pancreas cases. The results support that these procedures could be feasible and safe for preventing clinically significant POPFs after PD in hard pancreas cases. The authors propose that the characteristics of our procedures could be the reason for this benefit. Initially, instead of the conventional curved needle with a circumferential suture, a straight needle was used to minimize pancreatic laceration and parenchymal injury from needles or suture ligations. As described by Neychev and Saldinger [17], straightening the needle and using large needles with an increased radius would help to reduce the force required for passing the needle through the pancreas stump, and this could minimize the tissue deformation caused by the tangential shear stress of the needle. Second, 4 buttresses were introduced to minimize the gap between the jejunum wall and the pancreas, and this helped to make the anastomosis more secure. The buttresses could provide the required compressive force around the suture sites and reduce the space between adjacent stitches. We expect that the buttresses could also prevent the crushing of the pancreas tissue around the needle sites during tying. Furthermore, the buttresses could occlude the stitch holes on the anastomosis sites that were created by the needle. The potential gaps or the needle holes in the anastomosis could be one of the critical causes in the etiology of POPF as previously described by Torer et al. [18] and Peng et al. [19]. We propose that our use of buttresses could effectively help prevent POPF. Third, only two transpancreatic sutures were applied in our procedures, and the reduced number of sutures is expected to decrease the suture damage to the pancreas parenchyma and also reduce the risk of bleeding during the passage of the needle.

We have applied PJt anastomosis only for hard pancreas cases since 2013; however, the PGt anastomosis has also been selectively performed in patients with soft pancreases or the unusual condition in which there is a size mismatch between the pancreas and jejunum, such as in severe pancreatitis with edematous changes or with a bulky pancreas. In such cases, the enlarged pancreas stump is usually too hard to firmly invaginate into the lumen of the jejunum. Actually, in 2 patients, the method of anastomosis was changed to PGt from PJt during the operation. In this way, we selected the appropriate technique between PGt or PJt, and a tailored surgical approach could be employed based on the condition of the pancreas and viscera.

The results of this retrospective study should be interpreted with caution because of the study limitations. Selection bias could not be avoided, and there is concern that the type of anastomosis was chosen based on the surgeon's subjective judgment according to the clinical findings. To overcome these limitations, detailed indications and selection criteria for each anastomosis type should be accurately established. The current study also produced no data on the long-term outcomes related to pancreas exocrine insufficiency according to the type of anastomosis. The parameters related to digestive function should be evaluated in a future study to compare the exocrine function between the different types of anastomoses.

However, the PJt presented feasible and improved outcomes regarding POPF and the pancreaticoenteric anastomosis time despite these limitations. Moreover, this approach is also expected to be more easily applied in laparoscopic PD procedures. In previous reports using laparoscopic PD, the multiple sutures in the posterior pancreas wall has been the vulnerable point in the surgery due to the restrictions in suture motion, which is the one of fundamental limitations of laparoscopic surgery. However, in the case of PJt, only two transpancreatic sutures without additional reinforcements were sufficient to complete the anastomosis, which can reduce the operator burden even though it is only applicable in hard pancreas cases. The authors have performed 10 complete laparoscopic PDs successfully using this technique, although we did not describe those cases in this article.

In conclusion, we propose that this novel technique is very simple, easy, and safe for hard pancreas cases, and it is expected to have advantages over the conventional Du or PGt. We also expect that it could be useful for performing laparoscopic pancreaticoduodenectomies more comfortably. A well-designed randomized controlled prospective study with large sample sizes should be conducted in the near future to establish the superiority of this method over the conventional technique.