Although the role of laparoscopic distal pancreatectomy for neuroendocrine and cystic pancreatic neoplasms as well as for chronic pancreatitis is now well recognized and has been associated with a shorter postoperative hospital stay and a more rapid recovery [7], the application of laparoscopic surgery to the resection of periampullary tumors remains controversial. Laparoscopic pancreaticoduodenectomy (LPD) was first reported in 1992. Since then, the procedure has been attempted in 12 patients. The conversion rate for these cases was 33%, and no benefits to the patients in were observed terms of postoperative recovery and convalescence [5, 9, 11]. However, early experience with the hand-assisted approach has been promising [10].

We report what we believe to be the first UK experience with laparoscopic hand-assisted pancreaticoduodenectomy (LHAPD) in a patient with ampullary cancer. The procedure was uneventful, and the postoperative recovery was highly favorable.

Materials and methods

Patient

A 62-year-old man presented with a 2-week history of painless obstructive jaundice (serum bilirubin, 121 mmol/l) and a weight loss of several pounds. He had had an open appendectomy in childhood through a lower paramedian incision. He was otherwise fit and well, and at a height of 1.73 m and weight of 71.4 kg he had a body mass index (BMI) of 23.9 kg/m2.

Investigations at the referring hospital, including an abdominal ultrasonography, CT, and endoscopic retrograde cholangiopancreatography (ERCP), revealed an ampullary tumor with dilatation of the common bile duct to 10 mm in diameter and no pancreatic duct dilatation. There was no CT evidence of a tumor mass in the region of the head of the pancreas, no vascular involvement, and no hepatic or pulmonary metastases. Endoscopic biopsy samples of the ampullary tumor confirmed the diagnosis of an adenocarcinoma.

A 10F 5-cm straight plastic stent was inserted at ERCP at the referring hospital. The patient was then transferred to our specialist hepatopancreatobiliary and laparoscopic unit to undergo consideration for pancreatic resection.

Staging laparoscopy

Although we agree with others that a staging laparoscopy in patients with ampullary cancer is not routinely necessary [19], we wanted to ensure that there was no peritoneal spread before embarking on careful planning (consent, operating theater equipment, operating theater and recovery staff) for an LPD.

Laparoscopy was carried out using a three-port approach (with 5-mm ports) and a 30° telescope. It revealed omental adhesions to the abdominal wall from the previous appendectomy but no intraperitoneal metastases. Laparoscopic ultrasound was not used in this staging.

The patient made an uneventful recovery and was discharged home on the evening of surgery. He was scheduled to undergo LHAPD 2 weeks later.

Laparoscopic hand-assisted pancreaticoduodenectomy

General considerations

The procedure was carried out in June 2003 under general anesthesia and epidural analgesia, with preoperative bowel preparation and antibiotic cover. Low-molecular-weight heparin (LMWH) (Fragmin, 2,500 U) was administered subcutaneously after insertion of the epidural catheter and before beginning the operation. The patient wore graduated compression stockings, and intermittent pneumatic compression boots were applied to the lower extremities in the operating theater. The patient was catheterized and placed in the flat Lloyd-Davies position. Most of the operation was carried out with the patient tilted in a 30° reverse Trendelenburg position. We used three 5-mm and two 12-mm ports, and we made a 10-cm transverse incision in the right upper abdomen for a hand port (Gelport; Applied Medical Resources, Rancho Santa Margarita, CA, USA). The sites for port placement are shown in Fig. 1. The capnoperitoneum was set at 12 mmHg.

Figure 1
figure 1

Sizes and sites of placement of the laparoscopic ports and the hand port.

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Dissection and resection

The liver was retracted in a cephalic direction using an 80-mm angled Endoflex retractor (Surgical Innovations, Leeds, England, UK), which was fixed in position using a table clamp (Fastclamp; Snowden Pencer, Atlanta, GA, USA). With the surgeon’s left hand placed in the abdomen via the hand port, the dissection proceeded safely using a combination of a 5-mm ultrasonically activated scalpel (UAS) (Ethicon Endo-Surgery, Cincinnati, OH, USA) and the 5-mm Ligasure system (Valleylab, CO, USA).

The omental adhesions were first taken down; then, the gastrocolic omentum was divided, exposing the head of the pancreas. The right gastroepiploic vessels and the communicating vein between the middle colic and right gastroepiploic veins were secured with 10-mm endoclips (Ligaclip ERCA; Ethicon Endo-Surgery) and divided. The hepatic flexure was then taken down, and the duodenum was extensively kocherized, exposing the inferior vena cava and left renal vein and separating the third part of the duodenum from the transverse mesocolon. The inferior pancreaticoduodenal vein was exposed and divided between endoclips. The superior mesenteric vein was exposed and followed up to reveal its retropancreatic course and approach the origin of the portal vein (PV).

Attention was then directed to performance of a retrograde en bloc cholecystectomy, for which the UAS was employed. The cystic artery was secured with an endoclip and divided with the UAS. The hepatoduodenal ligament was dissected close to the hepatic hilum, exposing the right hepatic artery and revealing the common hepatic duct, which was divided with the UAS above the cystic duct insertion. The distal divided end of the bile duct, including the biliary stent that was displaced distally during manipulation, was closed with a continuous polydioxanone (PDS) 3-0 suture (Ethicon., Edinburgh, Scotland, UK). Dissection of the hepatoduodenal ligament was continued in a caudal direction, with division of the neurolymphatic channels and lymph nodes off the right hepatic artery and exposure of the common hepatic and gastrodudoenal arteries. The anterior hepatic lymph node (group 8a) was mobilized off the common hepatic artery and resected, and the gastrodudoenal artery was ligated proximally with Vicryl 3-0 (Ethicon., Somerville, NJ, USA), secured with endoclips, and divided. The PV was exposed, and its most superior tributary was divided between endoclips. The retropancreatic tunnel was then completed, separating the PV from the neck of the pancreas.

The right gastroepiploic vessels and the vascular arcade along the lesser curve of the stomach at the level of the incisura were divided between endoclips with the aid of the Ligasure and the UAS. The stomach was divided at the junction of the antrum with the body of the stomach (en bloc antrectomy) using three firings of an endo-stapler (ATB45 45-mm articulating; Ethicon Endo-Surgery).

Attention was then directed to the proximal jejunum, which was mobilized off the retroperitoneum and the inferior mesenteric vein using the UAS. The ligament of Treitz was divided. Then the jejunum was divided with an endo-stapler ~5 cm distal to the duodenojejunal flexure, and the divided ends of the bowel were oversewn with an invaginating continuous Vicryl 3-0 suture. The mesentery of the divided proximal jejunum was secured with the Ligasure and divided with the UAS. The mobilized and devascularized proximal jejunum was delivered to the supracolic subhepatic space. The neck of the pancreas was then divided at a level to the left of the PV. The UAS was used to divide the superior and inferior thirds of the neck of the pancreas to achieve a satisfactory hemostasis, and the middle third of the gland that harbored the nondilated pancreatic duct was divided using sharp scissors to avoid sealing the pancreatic duct with the UAS. The venous tributaries from the head of the pancreas to the PV were carefully dissected and divided between endoclips (Fig. 2). The superior mesenteric artery (SMA) could then be readily palpated; its branches to the head of the pancreas, including the inferior pancreaticoduodenal artery, as well as the neurolymphatics to the right of the SMA and some of the group 14 lymph nodes, were divided using endoclips and the 10-mm Ligasure.

Figure 2
figure 2

Intraoperative view after completion of the resection showing the common hepatic artery (1), the stump of the gastrodudoenal artery (2), the right hepatic artery (3), the portal vein (4), the inferior vena cava (5), and the divided stump of the common hepatic duct (6).

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The specimen was retrieved from the abdomen through the hand port and sent for histological analysis. The abdominal cavity was lavaged with 2 L of normal saline, hemostasis was confirmed, and the abdominal cavity was packed with gauze swabs. The operating table was returned to a neutral position, the hand port was removed, and the pneumoperitoneum was deflated for a 30-min break.

Throughout the operation, the pneumoperitoneum was deflated every 2–3 h for a 5–10-min period to enable the patient to recover from the physiological stress of prolonged capnoperitoneum [4].

Reconstruction

The reconstruction was fashioned in a Roux-en-Y manner with two retrocolic loops, each measuring approximately 50 cm in length. The discontinuous (isolated) and most posterior loop was used to fashion the pancreatic and biliary anastomoses. Both of these anastomoses were created using an interrupted, full-thickness, single-layer technique (PDS 3-0 sutures), and fashioned in an end-to-side manner.

A small window in the root of the transverse mesocolon was created to the right of the middle colic vessels, and the divided jejunum was delivered into the supracolic subhepatic space. A 9 F external pancreatic stent (75-cm fine-needle catheter, Freka FKJ/FCJ; Fresenius Kabi Deutschland, Bad Homburg, Germany) was introduced through the skin below the right costal margin at the midaxillary line using the supplied needle, which was then used to puncture the jejunal loop at a convenient point ~15–20 cm from the loop’s divided end. The stent was advanced through the lumen of the jejunum and exteriorized along the antemesenteric border ~3–4 cm proximal to the divided end of jejunum. The pancreatic anastomosis was constructed first and was placed most proximally on the jejunal loop. Eight interrupted sutures were deployed, and the anterior row was held in position with the aid of a suture-holding device (Gabbay-Frater Suture Guide, Genzyme, Neu-Isenburg, Germany) that was delivered into the abdominal cavity through the hand port. The posterior row of sutures was completed and tied. The pancreatic stent was advanced into the pancreatic duct for a few centimeters, and the anterior row of sutures were completed and tied (Fig. 3). The biliary anastomosis was constructed in a similar manner ~4–5 cm distally (Fig. 4). No T-tubes or stents were used across the biliary anastomosis. The point of entry of the external pancreatic stent into the jejunum was secured with a pursestring suture (PDS 3-0), and the loop was fixed to the lateral abdominal wall (PDS 3-0 sutures). Its site was marked with the application of large titanium clips to the abdominal wall; the clips were intended to act as markers for a potential access loop.

Figure 3
figure 3

Intraoperative view showing the completed end-to-side pancreaticojejunal anastomosis.

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Figure 4
figure 4

Intraoperative view showing the completed end-to-side hepaticojejunal anastomosis.

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A point on the jejunal loop ~50 cm distal to the biliary anastomosis was identified. The hand port was removed, the pneumoperitoneum deflated, and the relevant loop of jejunum delivered to the exterior through the hand port wound. The jejunum was then divided with a stapling device (TLC55; Ethicon Endo-Surgery). An extracorporeal side-to-side jejunojeunostomy was fashioned using a hand-sutured two-layer anastomosis with a continuous monocryl 3-0 (poliglecaprone 25; Ethicon., Edinburgh, Scotland, UK) suture technique.

The small bowel was returned to the abdomen, the hand port was replaced, and the pneumoperitoneum reestablished at 12 mmHg. The divided end of the continuous Roux loop was delivered retrocolically and more anteriorly through another mesenteric window, and an end-to-side gastrojejunostomy was fashioned using a posterior full-thickness seromuscular gastrojejunal continuous suture (monocryl 3-0) incorporating the gastric staple line, a stapled gastrojejunostomy parallel and ~2 cm proximal to the divided end of the stomach, and a continuous monocryl 3-0 suture to close the common opening between the stomach and jejunum (Fig. 5).

Figure 5
figure 5

Intraoperative view showing the completed end-to-side gastrojejunal anastomosis.

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Hemostasis was confirmed, all the mesenteric defects were closed with interrupted monocryl 3-0, and a 16F 150-cm triple-lumen nasojejunal feeding tube (Fresenius Kabi, Bad Homburg, Germany) was then introduced and advanced until its distal tip was placed several centimeters distal to the jejunojunal anastomosis. The abdominal cavity was thoroughly lavaged with warm normal saline, and two 28F Portex Robinson drains (SIMS Portex, Hythe, Kent, England UK) were placed on either side.

Results

Operation-related outcomes

The intraoperative course was uneventful, and the procedure was completed laparoscopically. The operating time was 11 h (plus a 30-min break between the resection and reconstruction phases). The estimated intraoperative blood loss was ~500 ml; 2 U of blood were transfused intraoperatively.

Postoperative course

The patient was extubated at the conclusion of the operation and transferred to the critical care unit, where he stayed overnight for 11 h. He was then returned to the ward. Nasojejunal feeding was started 12 h postoperatively using Nutrison (Nutricia., Trowbridge, Wiltshire, England, UK) at an initial rate of 30 ml/h. The feeding rate was increased gradually to a maximum of 75 ml/h on the 3rd postoperative day. Oral fluids were commenced on the 1st postoperative day at 30 ml/h, and an oral soft diet was started on the 3rd postoperative day. The nasogastric enteral feeding tube was removed on the 5th postoperative day.

The epidural analgesia was discontinued and removed on the 3rd postoperative day. A patient-controlled opiate-analgesia–based system was commenced at this time and was later discontinued on the 5th postoperative day. The patient was able to walk independently on the 4th postoperative day; the urinary catheter was then removed. The drain fluid was of low amylase concentration (12 U/L) on the 5th postoperative day, when the abdominal drains were removed.

The patient developed superficial pressure sores over the buttocks (Fig. 6A) and the posterior aspect of the elbows (Fig. 6B). They were managed with dressings and required no surgical intervention. He was discharged home on the 9th postoperative day with the external pancreatic drain in situ.

Figure 6
figure 6

Superficial pressure sores over the sacrum (A) and the back of both elbows (B) on the 10th postoperative day.

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Histology

Histological examination revealed an X-grade ampullary adenocarcinoma that measured 1.5 cm in diameter with clear pancreatic, biliary, and circumferential resection margins. A total of 13 lymph nodes were retrieved from the specimen and examined; two of them were involved with metastases (the anterior superior and inferior pancreaticoduodenal nodes, group 17a and 17b). The pathological stage was pT3 pN1 pMx.

Follow-up

The patient was reviewed in the surgical outpatient unit at 10 days and then again at 5 weeks, when his external pancreatic stent was removed. His wounds have healed satisfactorily (Fig. 7). He was randomized to the observation arm of the ESPAC 3 trial and remains well and disease-free some 2 months postresection. He is receiving adjuvant chemotherapy.

Figure 7
figure 7

Good healing of the wounds was achieved by the 10th postoperative day. The external pancreatic drain can be seen on the right side of the patient’s for so.

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Discussion

The introduction of the hand port to the practice of laparoscopic surgery has facilitated the safe and effective accomplishment of some complex laparoscopic operations. The world experience with laparoscopic hand-assisted liver resection [8], colonic resection [3], splenectomy for giant spleens [1], abdominal aortic aneurysm repair [6], donor nephrectomy [18], and other procedures has shown favorable results in terms of operating time, conversion rate, and postoperative patient recovery. Moreover, recent reports of two LHAPD for periampullary tumors have also shown favorable results [10, 13]. This positive experience is supported by our own results with this procedure. The recovery of our patient was markedly quicker, both in hospital and after discharge, than that observed at best with open PD.

The hand port offers advantages during both the resection and reconstruction phases of a LHAPD and facilitates retrieval of the specimen. The use of the hand port enables the surgeon to achieve adequate and safe tissue retraction, dissection, and rapid pressure control of bleeding, and it simplifies intracorporeal suturing and the fashioning of anastomoses. The benefits of an uncompromised tactile sensation in the identification of structures, such as the right hepatic and the superior mesenteric arteries, are maintained.

The role of extended lymphadenectomy, as advocated by most Japanese surgeons [14] in patients undergoing PD for periampullary cancer, remains controversial. In a randomized controlled trial by Yeo et al. [20] comparing standard vs radical (extended) PD in ~300 patients with periampullary adenocarcinoma, a significant increase was found in the incidence of overall complications with the radical approach, and no survival benefit was detected at a mean patient follow-up of 24 months. On the other hand, a small randomized controlled trial of a total of 81 patients suggested, in an unplanned subgroup analysis, a trend toward longer survival in node-positive patients treated with an extended rather than a standard lymphadenectomy [16]. The role of extended lymph node dissection in pancreatic cancer is currently being evaluated in a randomized controlled trial in Japan [14]. The extent of the lymphadenectomy that we applied was greater than that of a standard approach but did not include the full range of a radical lymphadenectomy. Nevertheless, the hand-assisted laparoscopic approach does facilitate an extended regional lymphadenectomy, as shown in a Japanese report of resection of gastric cancer [17].

Attention needs to be paid to the implications of prolonged surgery and pneumoperitoneum [4]. Our patient developed superficial pressure sores over the buttocks despite placement on a special gel mattress. The buttock injury might have resulted from a shearing force between the skin and the gel mattress caused by gradual slippage of the patient while he was in the reverse Trendelenburg position. Additional measures such as those used in bariatric surgery to prevent slippage of the patient and frequent neutralization of the patient–table position might be necessary. The physiological consequences of prolonged pneumoperitoneum and the reverse Trendelenburg position are well recognized [4] and may be minimized by operating under reduced insufflation pressure, administering LMWH perioperatively, using graduated compression stockings and an intermittent pneumatic compression device, and releasing the pneumoperitoneum intermittently [2, 15]. Heat loss and hypothermia becomes an issue during prolonged surgery, but it can be minimized by using general measures (Bair Hugger, fluid warmer, Blanketrol blankets) to warm the patient and the infused fluids. In addition, preventive measures specific to laparoscopic surgery include the minimization of gas leaks and the use of gas warming devices, although the benefit of the latter in achieving thermostasis has yet to be clearly demonstrated [12].

In selected patients with periampullary cancer, LHAPD is feasible and safe, and achieves satisfactory oncological clearance. Our initial experience with LHAPD was favorable, with apparent benefits to the patient. Attention, however, needs to be paid to the physiological consequences of prolonged laparoscopic surgery and the effects of deviation from a neutral (supine) patient position; preventive measures should be carefully applied. Future expansion in the applications and indications of LHAPD is likely.