Pitfalls for laparoscopic pancreaticoduodenectomy: Need for a stepwise approach

Abstract Because of today's advancements in surgical techniques and perioperative management skills, surgeons are beginning to explore the usefulness of the laparoscopic approach in managing periampullary tumors. However, as a result of its innate complexity and associated high surgery‐related complications, its applicability to the general surgical community remains controversial. To date, only retrospective data from high‐volume centers support the safety and feasibility of laparoscopic pancreaticoduodenectomy (Lap PD) for the treatment of benign conditions and malignant periampullary tumors. In addition, various surgical techniques in terms of port placement, dissection, and reconstruction have evolved in different centers depending on the preferred method commonly used by the surgeon through accumulated experience. In our center, we used a stepwise approach and standardized our surgical technique to overcome this technically demanding procedure. A collaborative implementation of video review and analysis, practice training and simulation, operating room didactics, and strict adherence to our stepwise approach in Lap PD, might potentially improve the surgical skills of young hepatobiliary surgeons and possibly overcome the volume‐based learning curve of Lap PD.

Nevertheless, with today's advancements in surgical techniques and perioperative management skills, Lap PD is thought to be an appropriate approach for treating periampullary pathological conditions, particularly in high-volume centers. 5 With proper selection criteria and wise intraoperative decision-making for open conversion, Lap PD can be safely implemented in daily clinical practice.
Most importantly, standardization of various surgical techniques might be the key to overcome their innate complexity. Therefore, we describe our surgical technique and apply a stepwise approach as a benchmark to overcome the pitfalls of Lap PD.

| IND I C ATI ON S FOR L AP -PD
Surgical indications for Lap PD may be similar to those for Open PD. [6][7][8] Benign and low-grade malignant (borderline malignant) periampullary tumors are the best indications for Lap PD when considering long-term survival and quality of life, as minimal or no lymphadenectomy is needed. 9 Cases with periampullary cancers should be selected cautiously, because, in general, Lap PD may be technically very difficult in patients with severe obesity, severe cholangitis, pancreatitis, and potential risk of combined major vascular resection. Particularly when dealing with mid-bile duct cancer, resection-margin problems can occur during the operation, which make Lap PD more difficult, require longer operation time to obtain an additional margin for curative resection, and possibly decrease oncological benefit. However, it should be emphasized that surgeon expertise and experience in Lap PD can influence whether the patient undergoes the procedure. For instance, vascular resection can be carried out in a high-volume center with well-experienced surgeons. [10][11][12][13] For these reasons, patients with comorbidities and in poor general condition who cannot tolerate a lengthy pneumoperitoneum would find it difficult to undergo Lap PD.
Nevertheless, we standardized our Lap PD selection criteria for patients with periampullary tumor. Whether to carry out Lap PD or Open PD can be decided preoperatively or intraoperatively. In general, we select patients with benign and low-grade malignant periampullary lesions, periampullary cancer not involving major vascular structure, and good performance status as good candidates for Lap PD. Intraoperatively, wise decision-making for open conversion to laparotomy is paramount. For patient safety, failure to progress within 1 hour of dissection as a result of severe pancreatitis or adhesions, unexpected vascular invasion, unexpected adjacent organ involvement requiring combined organ resection, unusual vascular anatomy, and uncontrolled bleeding may warrant open conversion to laparotomy. 6 Although combined segmental resection of the major venous system is feasible and safe, 14 only expert surgeons can carry out this difficult intraoperative situation to complete a safe and successful Lap PD. Figure 1 illustrates the indications and basis for selection of Lap PD.

| E X TENT OF SURG I C AL D ISS EC TI ON
Standard dissection during PD is thought to be optimal when carrying out Lap PD.
There are several important randomized controlled studies comparing extended and standard dissection in periampullary cancer.
F I G U R E 1 Indications and basis for selection of laparoscopic pancreaticoduodenectomy (Lap PD). *Only expert surgeon can carry out this level of difficulty during Lap PD Most of the studies concluded that there was no survival benefit from carrying out extended lymphadenectomy compared to standard lymphadenectomy. [15][16][17] Recently, Jang et al 18 reported on a Korean multicenter collaborative study and concluded that there was no survival advantage in carrying out extended PD compared to standard PD. In their study, standard resection included dissection of lymph node stations 12b, 12c, 13, and 17 without nerve dissection around the hepatic artery or superior mesenteric artery (SMA), whereas extended resection included removal of lymph node stations 8, 9, 13, 17, 12, 14, and 16. Moreover, the nerve plexus or ganglion on the right side of the celiac axis and SMA was dissected semicircumferentially. These findings are the same as the results from a multicenter randomized controlled trial from Japan that failed to show survival benefits in patients undergoing extended PD compared to standard PD. 19 Therefore, based on currently available evidence and surgical techniques of Lap PD, standard dissection is feasible when carrying out Lap PD. However, extended dissection including para-aortic lymph nodes and perineural soft tissue around the SMA is allowed for margin-negative resection in selected cases and by selected expertise.

| P ORT PL ACEMENT AND OPER ATING ROOM S E T TING
Placement and number of trocars varied across centers. The number of trocars varied from five to seven. [20][21][22] Depending on the surgeon's preference, it is most important that the surgeon can manipulate the instruments ergonomically and achieve the best exposure. Our approach in Yonsei, however, used six to seven trocars, as presented in Figure 2

| Devices
Three laparoscopic graspers, two laparoscopic dissectors, and one laparoscopic needle holder with straight plastic handles were used for Lap PD. Ultrasonic (recently referred to as a vessel-sealing system) and bipolar energy devices are fundamental requirements for Lap PD. A bipolar energy device is especially useful in blunt dissection and for complete coagulation around major vascular structures.

| S TEPWIS E APPROACH TO L APAROSCOPI C PAN CRE ATICODUODENEC TOMY
Different surgical techniques in terms of port placement, dissection, and reconstruction have been reported in different high-volume centers. 21,[23][24][25][26][27][28][29] As such, standardization of an operative technique may vary across regions or countries depending on the prepared method commonly used by the surgeon. However, it should be emphasized that implementation of a standard protocol is paramount to overcome the volume-based learning curve for Lap PD. 30,31 Moreover, innovative training strategies should also be implemented for training young surgeons in the field of pancreatic surgery. 32 Recently, we began to explore the feasibility of laparoscopic pancreaticoduodenectomy for treating periampullary tumor and began to standardize our surgical technique. 14,[33][34][35] In our center, to augment hepatobiliary surgical training, we strictly implemented video review and analysis, practice training and simulation, operating room didactics, and strict implementation of our stepwise approach in Lap PD.
In a stepwise approach, Lap PD consists of the "resection phase" and the "reconstruction phase." Each is subdivided into a series of steps to guide the beginner's approach to Lap PD (Table 1).
According to tissue condition, the operation sequence may be changed, but the step-by-step approach in Table 1 will guide beginners through a safe and effective Lap PD.

| Division of the gastrocolic ligament
An incision is made into the gastrocolic ligament a few centimeters from the gastroepiploic arcade of the body of the stomach, using a LigaSure instrument (Medronics Inc, Boulder, Colorado, USA). By doing this, the left-hand grasper of the operator grasps the stomach while the assistant left-hand grasper retracts the colonic side to create an effective tension for dissection ( Figure 3). The dissection will F I G U R E 2 Placement of trocars and operator position. The surgeon stands at the right side of the patient during the entire surgical procedure. The laparoscopic camera is usually introduced through right-sided 12-mm ports (A and B) according to the target surgical field by Assist 1. Port a and port A (or B) will be the main working ports for the surgical procedure. Assist 2 can help to expose the surgical field using Ports b, c, and C. Port d can be added in case of robotic reconstruction. Two monitors (M1 and M2) are placed on the opposite side of the surgeons and nurses for ergonomic surgical interventions be continued up to the left gastroepiploic artery arcade. In this area, carrying out the procedure becomes much easier when the assisting surgeon lifts the stomach, because the surgeon can then use two hands for effective dissection. The gastrocolic ligament is further divided along the same plane toward the pyloric area to expose the right gastroepiploic vessels.

| Control of the right gastroepiploic vessels
The assistant lifts the stomach in a 12 o'clock position to properly expose the pyloric area. This will clearly expose the right gastroepiploic vessels, which can be effectively ligated using laparoscopic clips. Either individual control of the artery and the vein or simultaneous control of these vessels is acceptable. This will also facilitate dissection and separation of the antero-superior part of the head of the pancreas and the inferior part of the first portion of the duodenum ( Figure 4). Bleeding is usually encountered in this area and can be effectively controlled using laparoscopic clips and a bipolar energy device. When dissecting and controlling the right gastroepiploic vessels, removing too many of them from the stomach will result in vascular insufficiency around the duodenal stump, which would prevent a duodenojejunostomy.

| Control of the right gastric vessels
Next, the superior part of the first portion of the duodenum is dissected. The assistant right-hand grasper retracts the liver while the assistant left-hand grasper retracts the first portion of the duodenum to expose the hepatoduodenal ligament. The peritoneal lining of the hepatoduodenal ligament is incised just above the first portion of the duodenal wall and along the lesser curvature of the stomach antrum to expose the right gastric artery (RGA, Figure 5).
Once identified, it can be secured with laparoscopic clips and transected. For procedural efficacy, origin of the RGA should not be identified at that time. Instead, it can be identified and controlled during the stage of hepatoduodenal ligament dissection. In some cases, the left hepatic artery from the left gastric artery runs within the lesser sac. This vessel needs to be preserved in case of unexpected potential complications requiring total embolization of the hepatic artery as a result of gastroduodenal artery stump bleeding.

| Dissection of the superior border of the pancreatic neck
The left-hand grasper of the assistant will pull down the mesenteric attachment of the inferior border of the pancreas to allow a clear view of the superior border of the pancreas. The peritoneal lining of the hepatoduodenal ligament is incised along the pancreatic neck. Once opened, the common hepatic artery is usually identified and can be followed caudally to expose the gastroduodenal artery. The portal vein can be identified and exposed by dissecting the triangular-shaped tissue bordered by the common hepatic artery, gastroduodenal artery, and superior border of the neck of the pancreas (Figure 7). This can be facilitated by coagulation and blunt dissection of the fatty tissues around this area using a bipolar energy device.

| Dissection of the inferior border of the pancreatic neck
The transected right gastroepiploic vein can be followed down to its origin to identify the location of the superior mesenteric vein (SMV).
Once the SMV is identified, the left-hand grasper of the assistant holds the right dorsal part of the mesentery just caudal to the origin TA B L E 1 Stepwise approach for laparoscopic pancreaticoduodenectomy Resection stage Step 1 Division of the gastrocolic ligament Step 2 Control of the right gastrocolic vessels Step 3 Control of the right gastric artery Step 4 Transection of the first portion of the duodenum Step 5 Dissection of the superior border of the pancreatic neck Step 6 Dissection of the inferior border of the pancreatic neck Step 7 Creation of the pancreatic window and taping Step 8 Dissection of the hepatoduodenal ligament and common hepatic duct taping Step 9 Dissection of the pancreatic head and colonic mesentery Step 10 Mobilization of the duodenum and pancreatic head and division of the ligament of Treitz Step 11 Division of the proximal jejunum and control of mesenteric vessels Step 12 Division of the pancreas and uncinate process dissection Step 13 Division of the bile duct Reconstruction stage Step 1 Pancreaticojejunostomy anastomosis Step 2 Hepaticojejunostomy anastomosis Step 3 Extracorporeal duodenojejunostomy of the right gastroepiploic vein on the SMV. By doing this, the SMV can be clearly exposed for further dissection. The peritoneal lining on the antero-inferior aspect of the neck of the pancreas is dissected along the adventitia of the SMV, clearing all fatty tissues around it up to the inferior border of the pancreas (Figure 8). Small tributaries of the SMV might be encountered during dissection and can be safely secured using laparoscopic clips.

| Pancreatic neck window and taping
Once the dissection reaches the inferior border of the pancreas, right-angled dissector can now be inserted along this window up to the superior border of the neck of the pancreas (Figure 9).
Once the dissector visualizes the superior border of the pancreas, a tape is placed around the neck of the pancreas to facilitate later transection. The CBD is then dissected, separated from the portal vein, and circled and secured by tape ( Figure 10D).

| Dissection of the pancreatic head and colonic mesentery (control of the gastrocolic trunk)
Proper orientation of the head and body of the pancreas is one of the key points during this procedure. The avascular plane of the anterior aspect of the transverse mesocolon is followed to the head of The anterior inferior pancreaticoduodenal vein on the right lateral side of the RGEV can also be identified to its origin in the gastrocolic trunk ( Figure 11). With a combination of blunt and sharp dissection, the gastrocolic trunk is followed up to the SMV, which can be safely ligated with laparoscopic clips.  Small tributaries of the SMV might be encountered during dissection and can be safely secured using laparoscopic clips.

Para-aortic lymph node sampling
In cases where there were some enlarged lymph nodes around the para-aortic area, the lymph nodes and some connective tissues anterior to the inferior vena cava and aortocaval (station 16a and 16b) area were sampled for frozen section biopsy ( Figure 14).

| Pancreas division and uncinate process dissection
Next, the tape around the neck of the pancreas is pulled up at a 12 o'clock position. An energy device is used to partially transect the pancreas up to its duct, after which the transection is continued using scissors ( Figure 16). This procedure will be associated with some bleeding from the transected pancreatic surface parenchyma but can prevent the sealing of the small pancreatic duct. Bleeding can be controlled using a bipolar device or an electrocautery device.  Figure 17A). This artery should be ligated using laparoscopic clips, and dissection is continued along the lateral border of the SMA. Likewise, ICG used during this dissection can clearly define the border of the uncinate process and the retroperitoneal resection margin of dissection 33 ( Figure 17B-D). The left-hand grasper retracts the SMV superomedially to expose the soft tissues along the lateral border of the SMA. All connective tissues along the lateral wall of the SMA are dissected using a harmonic device.
Small vessels can be secured with laparoscopic clips.

| Division of the bile duct
After the head of the pancreas is free, the proximal portion of the common hepatic duct is clipped with a bulldog clamp to avoid bile spillage after transection while the distal portion is clipped with a hemoclip or bulldog clamp. The common hepatic duct is transected just above the origin of the cystic duct using scissors ( Figure 18). The specimen is placed into an endo-pouch. Cholecystectomy will be the last step in the resection phase for effective liver retraction to the end of the resection phase.

| Reconstruction stage
This stage is believed to be one of the biggest obstacles to wide application of Lap PD in clinical practice. However, when surgeons know the basic surgical principles for pancreaticojejunostomy (PJ) and hepaticojejunostomy (HJ) and some technical tips, these procedures can be safely carried out. In the near future, robotic surgical systems will play a large role in this stage. However, as a result of its high cost, not every patient can undergo robotic surgery. Therefore, pancreatic surgeons must have good surgical skills to undertake these challenging surgical procedures to fulfill the goal of minimally invasive surgery.

| Managing remnant pancreas
This step is the most challenging. However, through didactics and simulation, this step can be safely conducted. Instruments must be handled carefully to avoid cutting and injury to the pancreatic remnant during the anastomosis. Usually, four stitches are applied for a <2-mm pancreatic duct-to-mucosa PJ. For a duct >2 mm, six or more sutures can be used depending on the size of the duct. Achieving an exact angle of the needle is one of the most difficult steps during anastomosis. The following steps are our surgical strategy in managing the remnant pancreas during Lap PD.

1.
Interrupted suture, two-layer, duct-to-mucosa PJ with a short stent is our standard approach for managing the remnant pancreas.

2.
A laparoscopic camera is placed through Port B, using Port a and Port A as working ports to allow a more ergonomic position.

3.
The jejunal limb is brought to the pancreatic stump in a retrocolic way. In specific cases, the jejunal limb can be pulled up through the retromesenteric window.

7.
Once the duct-to-mucosa anastomosis is achieved, the anterior layer is completed using interrupted sutures from superior to inferior border pancreas.
Rotation with a blunt angle-fashioned needle mounted on a laparoscopic needle holder is carried out allowing a curving (spiral) movement for appropriate PJ suturing. Figure 19 shows the steps in pancreaticoduodenal anastomosis.

| Managing bile duct reconstruction
Posterior continuous and anterior interrupted sutures are placed for hepaticojejunostomy ( Figure 20). Using different types of suture materials; for example, multifilament absorbable sutures and monofilament absorbable/non-absorbable sutures, makes it much easier to differentiate between two stitches in a narrow surgical space. Tension should be carefully checked to avoid disruption of the anastomosis and bile leak. We usually use a 15-cm jejunal limb from the PJ site to avoid tension.

| Duodenojejunostomy
The umbilical wound (Port-A site) is extended by approximately 5 cm, which is enough to accommodate extraction of the specimen. A 50-cm Roux-en-Y limb of the jejunum from the hepaticojejunostomy site is marked for the duodenojejunostomy. The duodenum and jejunum must be carefully oriented laparoscopically, tagged with sutures, and removed through the small umbilical wound for anastomosis. End-toside or side-to-side duodenojejunostomy can be carried out manually. Figure 21 shows the postoperative wound after Lap PD. TA B L E 2 (continued)

| MERG ING I CG TECHNOLOGY IN PAN CRE ATI C SURG ERY
In Lap PD, initially reported by Rho et al, 34 ICG can identify adequate perfusion of the pancreas at the pancreaticojejunostomy anastomotic site by measurement of tissue fluorescence after injection during Lap PD. ICG was then used, in certain circumstances, to determine the appropriate surgical plane for dissecting the retroperitoneal margin, as it can be well identified with ICG technology. 33 However, further studies need to be undertaken to prove this usefulness. Nevertheless, since then, our center has used ICG as an adjunct to properly identify the plane of dissection in the uncinate process of the pancreas and on the lateral margin of the SMA.

| SUMMARY OF RE TROS PEC TIVE S TUD IE S OF THE FE A S IB ILIT Y AND SAFE T Y OF L AP PD
Recently, a number of retrospective studies evaluating the efficacy of Lap PD have been carried out 21,37-41 (Table 2). These studies included more than 50 cases of Lap PD in a single-institution series. Operative time ranged from 220 minutes to 810 minutes, with operative blood loss ranging from 45 mL to 8500 mL. Length of hospital stay ranged from 4 to 69 days depending on the associated morbidity after surgery. Vascular resections were also carried out. 37 In addition, the rate of pancreatic fistula was 10.1%. The rate of conversion to open PD was 2.9%. R0 resection rate ranged from 84% to 100%. All of the studies concluded that Lap PD is safe and feasible, especially when carried out in a high-volume center by experienced surgeons. Moreover, the Lap PD procedure in these case series was done by well-experienced and expert surgeons in the field of pancreatic surgery. More importantly, these surgeons were able to standardize their approach, perhaps as a result of their cumulative experience in laparoscopic surgery.

| CON CLUS ION
Although open PD remains the standard treatment for benign and malignant periampullary tumors, it is cautiously thought that Lap PD can be a good alternative option for well-selected patients with experienced laparoscopic pancreatic surgeons. The innate complexity of the procedure itself is the main pitfall of Lap PD.
However, for Lap PD to become accepted as safe and feasible in general, standardization of the procedure is paramount. Our collaborative strategy of outside-the-operating room didactics and simulation and inside-the-operating room step-by-step mastery of the lap PD procedure may considerably overcome the volumebased learning curve of lap PD.

ACK N OWLED G EM ENT
Parts of the manuscript were presented at the 73rd General Meeting of the Japanese Society of Gastroenterological Surgery (JSGS) in Kagoshima, July 2018.

D I SCLOS U R E
Conflicts of Interest: Authors declare no conflicts of interest for this article.