Total Laparoscopic Pancreaticoduodenectomy Using a New Technique of Pancreaticojejunostomy with Two Transpancreatic Sutures with Buttresses

Abstract

Background:

Laparoscopic pancreaticoduodenectomy is advantageous as a minimally invasive surgery, but performing the complicated anastomosis is technically difficult. Herein, we present our experiences with total laparoscopic pancreaticoduodenectomy (TLPD) using a unique anastomosis technique, that is, pancreaticojejunostomy using only two transpancreatic sutures with buttresses method (PJt).

Materials and Methods:

From September 2013 to March 2015, 12 TLPDs using PJt for periampullary tumors were performed. In each case, the pancreaticoenteric anastomosis was performed using the PJt technique, a modification of invaginated, end-to-end pancreaticojejunostomy. A pair of transpancreatic sutures were placed on the upper and lower borders of the implanted pancreas through the jejunal limb covering the pancreas stump, and four buttresses were used to reinforce the anastomosis. All medical records and follow-up data were reviewed and analyzed with regard to surgical outcomes, and the results were compared with previously published reports on TLPD.

Results:

The mean age of the patients was 64.3 ± 12.3 years, and all were diagnosed with pancreas head cancer except 5 patients (4 patients had ampulla of Vater cancer, and the other had chronic pancreatitis). The mean estimated blood loss was 118 ± 57 mL, and the mean hospital stay was 12.5 ± 4.5 days. The mean operative time was 411.6 ± 59.2 minutes, and the pancreas anastomosis time was 20.1 ± 4.8 minutes without any evidence of anastomosis-related complications.

Conclusions:

Our novel technique of PJt is a simple, easy, and feasible method for TLPD with the possibility of reducing the burden to the operator and acquiring secure anastomosis.

Introduction

Laparoscopic surgery has been widely accepted for various surgeries due to the advantages of minimally invasive procedures. The number of distal pancreatectomies for tumors in the pancreas body or tail has increased in the last decade.¹ However, for periampullary tumors, laparoscopic pancreaticoduodenectomy (LPD) is still considered a conundrum because of its technical difficulties, particularly the complicated anastomosis that is required. Therefore, only a few, very specialized pancreatic surgeons have performed total LPD (TLPD), and reports on TLPD have been limited.² Recent advancements in laparoscopic techniques and instruments have encouraged pancreatic surgeons to attempt minimally invasive surgery of periampullary tumors,^3–5 but this type of surgery remains challenging for most surgeons.

Since April 2014, we have performed TLPD using a unique pancreaticoenteric anastomosis technique, that is, pancreaticojejunostomy using two transpancreatic sutures with buttresses method (PJt method). Herein, we describe our experience with TLPD using PJt and evaluate the surgical outcomes and feasibility of the method.

Materials and Methods

From March 2009 to March 2015, in total, 61 LPDs for periampullary tumors were performed at the Department of Hepato-biliary and Pancreas Surgery, Seoul St. Mary's Hospital. In most cases, the pancreas anastomosis was performed using minilaparotomy after the completion of the resectional stage and hepaticojejunostomy via a laparoscopic approach.⁶ TLPD using PJt was first performed in September 2013 and thereafter consistently applied to the pancreaticoenteric anastomosis of TLPD cases performed by Surgeon H. In cases of malignancy, only limited cancers without distant metastasis were treated using the laparoscopic approach, and the cases showing invasion or proximity to main vessels such as the portal vein, superior mesenteric vein, common hepatic artery, or superior mesenteric artery were excluded. Cases with evidence of acute pancreatitis on preoperative imaging and operative findings or requiring concomitant surgery for other organs were operated on using the open method. All patients were informed about the possible advantages and complications of laparoscopic surgery, and informed consent was obtained.

All medical records and follow-up data were reviewed and analyzed with regard to surgical outcomes and then compared with the results of previously published reports about TLPD. Operative outcomes (overall operative time, pancreas anastomosis time, estimated blood loss, and intraoperative transfusion) and postoperative results (length of hospital stay, start of oral diet, postoperative pain calculated using the visual analog scale, postoperative morbidities, and mortality) were prospectively determined and analyzed retrospectively.

Operative technique

Five trocars were generally used, and the port locations are shown in Figure 1. One 10-mm umbilicus trocar for the laparoscope port, one 12-mm trocar on the right flank for the right hand of the operator, one 10-mm trocar on the left midclavicular line for the right hand of the first assistant, and two additional 5-mm trocars (one on the left flank for the left hand of the first assistant and the other on the right midclavicular line for the left hand of the operator) were used.

FIG. 1.

(A) The locations of the five trocars. (B) View of the completed resection stage. For lymph node dissection in the case of malignancy, the range of dissection included the lymphoid tissues around the peripancreatic area, the inferior vena cava, the aorta, the common hepatic artery, the proximal 0.5–1 cm of the celiac axis and portal vein, and the right side of the superior mesenteric artery.

The operative procedures for pancreaticoduodenectomy were similar to those for conventional open pancreaticoduodenectomy. The pancreas neck transection was performed using electrocautery and scissors with caution to avoid injury of the pancreatic duct. In cases of malignancy, radical lymph node dissection was performed using ultrasonic coagulating shears, and the range of dissection included the lymphoid tissues around the peripancreatic area, the inferior vena cava, the aorta, the common hepatic artery, the proximal 0.5–1 cm of the celiac axis and portal vein, and the right side of the superior mesenteric artery. We skeletonized these structures individually up to the porta hepatis (Fig. 1).

After the resection stage was completed, the specimen was bagged, and irrigation was performed. For all cases of TLPD, we used this PJt anastomosis. The pancreas remnant stump was dissected approximately 3–4 cm in length from the splenic vein and retroperitoneal attachments. Small vessel branches between the pancreas and splenic vein or superior mesenteric vein were managed with ultrasonic coagulating shears (Harmonic Ace^® scalpel; Ethicon Endo-Surgery, Inc., Cincinnati, OH). The location of the main pancreatic duct was identified, and a short plastic stent was inserted at least 4 cm into the duct to prevent compression of the duct during the tying of the transpancreatic sutures or accidental suture of the duct. Two stay sutures were placed on both corners of the pancreas stump for traction of the pancreas stump into the jejunal lumen.

After the preparation of the pancreas stump, a small hole in the jejunum was made on the antimesenteric side for the hepaticojejunostomy, and the laparoscopic instrument at the RUQ area was brought into the hole through a 5-mm trocar. The stay sutures on the pancreas were then grasped and gently pulled until the pancreatic stump was implanted into the jejunum approximately 3–4 cm (Fig. 2). Two transpancreatic sutures with buttresses were subsequently placed intracorporeally on both the upper and lower borders of the implanted pancreas through the jejunal limb, which covered the pancreas (Fig. 3). This suturing required a pair of 4-0 monofilament polyprolene threads with a half-curved needle at each end (4-0 Prolene^®; Ethicon Inc., Somerville, NJ) and four buttresses (tetrafluoroethylene polymer pledget; Ethicon Inc.). The suture was first passed straight from the posterior surface of the covered jejunal limb and then penetrated the full thickness of the implanted pancreas at a level 2 cm below the cut surface, from the dorsal surface to the ventral surface. Then, it passed straight through the anterior surface of the covered jejunal limb. The buttresses were then inserted through each needle, and the anastomosis was completed with a knot that included the entire jejunal wall and implanted pancreas.

FIG. 2.

View of the implanted pancreatic stump in the jejunum. After the pancreas stump was prepared, a small hole in the jejunum was made on the antimesenteric side where the hepaticojejunostomy would be performed, and the laparoscopic instrument was brought into the hole. The stay sutures on the pancreas were grasped, and the two stay sutures were pulled until the pancreatic stump was implanted approximately 3–4 cm into the jejunum.

FIG. 3.

The view of the two transpancreatic sutures with buttresses on both the upper and lower borders of the implanted pancreas: (A) schematic diagram and (B) operative view.

To facilitate the pancreaticojejunostomy, the surgeon who stood at the right of the patient made the first transpancreatic suture at the lower border of the pancreas in the dorsal to ventral direction of the pancreas. The surgeon used two trocars on the right side of the patient (12-mm trocar for the right hand of the operator, 5-mm trocar for the left hand of the operator) for favorable ergonomics to allow comfortable laparoscopic suturing. After completing the first suture, the operator moved to the left side of the patient and then performed the second suture at the upper border of the pancreas in the dorsal to ventral direction; two trocars on the left side of the patient were used for this second suture (10-mm trocar for the right hand of the operator, 5-mm trocar for the left hand of the operator). No additional reinforcement sutures were placed on the anastomosis line. After the pancreaticojejunostomy was completed, an end-to-side choledochojejunostomy was performed with a single-layer continuous suture using absorbable 4-0 coated monofilament sutures by the anterior raw edge and the posterior raw edge individually. An antecolic, end-to-side duodenojejunostomy with a hand-sewn technique or side-to-side gastrojejunostomy using a stapler was also performed intracorporeally.

After reconstruction of the digestive tract was complete, the specimen was retrieved through an umbilical trocar site with a minimal extension of approximately 3 cm in length. Two closed suction drains were used: one for the pancreaticojejunostomy site through the left-sided 5-mm port incision and the other for the choledochojejunostomy site through the right flank port site.

Postoperative management and outcome assessment

A nasogastric tube was routinely inserted at the beginning of surgery and removed as soon as possible if the drainage was less than 100 mL/day. All patients were given parenteral nutritional support beginning on the day after the surgery if vital signs were stable; nutritional support was continued until oral feeding could begin. On postoperative Day 5, patients were routinely evaluated by abdomen computed tomography scans, and if there was no evidence of anastomosis leakage on both the computed tomography scan and clinical signs, oral feeding was resumed. Subcutaneous somatostatin therapy was not administered routinely in the postoperative period unless definite evidence of leakage was observed. In each case, the operative time was defined as the duration from skin incision to closure. The pancreas anastomosis time was specified as the time from the completion of the resectional stage to the completion of the pancreaticoenteric anastomosis with the last knot and included procedures such as mobilization of the pancreas stump, invagination of the pancreas stump to the jejunum, and performing two transpancreatic sutures with buttresses. Time not related to the progress of surgery, such as the irrigation time, was excluded. The operative time and pancreatic anastomosis time were accurately calculated using video and operative records.

Postoperative morbidities were reviewed and graded from 0 to 5 by using the Clavien–Dindo classification.⁷ According to this classification system, Grade I complication means any deviation from the normal postoperative course without the need of any pharmacologic treatment or interventions. Grade II complications are defined as the cases that require pharmacologic treatment, total parenteral nutrition, or blood transfusion. Grade III complications are any cases that require endoscopic, radiologic, or surgical interventions. Grade IV complications are defined as life-threatening morbidities, and Grade V complications represent the death of a patient.

According to the International Study Group of Pancreatic Fistula definition,⁸ postoperative pancreatic fistula (POPF) was defined as the drainage of any significant volume on postoperative Day 3 or later with an amylase concentration more than three times the normal serum amylase concentration. Each POPF was classified as Grade A, B, or C according to the following International Study Group of Pancreatic Fistula criteria: Grade A POPF is clinically stable and requires no treatment or admission, and therefore it is not considered as a morbidity; Grade B POPF has fluid collection on computed tomography scan and may require treatment and/or readmission; and Grade C POPF is clinically unstable and requires treatment or reoperation, and sepsis or infection may be present. In this study, we considered only Grade B and C POPF to be clinically significant.

Drains remained in place for at least 5 days after surgery, and the properties and volumes of the drains were recorded. Drains were removed when the amylase concentration of the drainage decreased gradually and there was no sign of POPF or intraabdominal infection.

The considerations for discharge were as follows: fine condition, tolerable pain with oral analgesics, and proper resumption of oral diet. Patients returned to the surgical outpatient department on Day 7 after discharge for an evaluation of general condition and then every 3–6 months for surveillance of tumor recurrence distinct from the course of adjuvant management.

Results

The demographic characteristics and surgical outcomes of TLPD are summarized in Table 1. The mean age of the patients was 64.3 ± 12.3 years, and all were diagnosed with pancreas head cancer except 5 patients, 4 of whom had ampulla of Vater cancer and the other had chronic pancreatitis. Most patients who were diagnosed with pancreas head cancer and chronic pancreatitis presented with a hard pancreas stump (7/12, 58.3%), whereas the other patients had a soft pancreas stump (5/12, 41.6%). The mean estimated blood loss was 118 ± 57 mL, the return to oral diet began on postoperative Day 4.5 ± 0.6 on average, and the mean length of hospital stay was 12.5 ± 4.5 days (Table 2). There were no cases of conversion to laparotomy during the operation or hospital mortality in the current study. Except for minor complications such as trocar-site infection or urinary difficulties, clinically significant morbidities including Grade B or C POPF were not observed in this study. The mean operative time in this study was approximately 411.6 ± 59.2 minutes, and the pancreas anastomosis time was short (20.1 ± 4.8 minutes) without any evidence of anastomosis-related complications. In terms of pathological outcomes, the mean tumor size and mean length of the harvested specimens were estimated as approximately 2.9 ± 0.4 (range, 2.0–3.8) and 25.3 ± 2.6 (range, 21.0–29.0), respectively. The mean number of harvested lymph nodes was 14.2 ± 2.3 (range, 11–17), and the mean number of lymph nodes that were positive for malignancy was 4.7 ± 2.5 (range, 2–7).

Table 1.

Demographic Features and Operative Outcomes for All Patients Undergoing Total Laparoscopic Pancreaticoduodenectomy with Pancreaticojejunostomy Using Only Two Transpancreatic Sutures with Buttresses Method

						Operative outcomes
Patient	Age (years)/sex	ASA class	BMI (kg/m²)	Diagnosis	Nature of pancreatic stump	Operative time (minutes)	Pancreas anastomosis time (minutes)	EBL (mL)	Conversion to laparotomy
Case 1	68/M	1	22.0	Pancreatic cancer	Hard	570	30	100	No
Case 2	71/F	2	21.3	Pancreatic cancer	Hard	390	23	75	No
Case 3	43/F	1	22.4	AOV cancer	Soft	410	24	75	No
Case 4	46/F	2	31.9	Chronic pancreatitis	Hard	340	15	125	No
Case 5	76/F	3	23.5	Pancreatic cancer	Hard	430	15	50	No
Case 6	81/M	3	25.2	Pancreatic cancer	Hard	390	17	130	No
Case 7	78/M	3	20.8	Pancreatic cancer	Hard	420	19	75	No
Case 8	52/M	1	21.7	Pancreatic cancer	Soft	450	25	100	No
Case 9	63/F	2	20.8	AOV cancer	Soft	360	15	90	No
Case 10	58/M	1	20.9	AOV cancer	Soft	420	20	200	No
Case 11	67/M	1	22.3	Pancreatic cancer	Hard	400	16	250	No
Case 12	69/F	2	21.5	AOV cancer	Soft	360	23	150	No

AOV, ampulla of Vater; ASA, American Society of Anesthesiologists; BMI, body mass index; EBL, estimated blood loss; F, female; M, male.

Table 2.

Postoperative Outcomes for All Patients Undergoing Total Laparoscopic Pancreaticoduodenectomy with Pancreaticojejunostomy Using Only Two Transpancreatic Sutures with Buttresses Method

			Postoperative pain (VAS)			Amylase level (IU) in drain
Patient	Length of hospital stay (days)	Start of oral diet (POD)	POD 1	POD 3	POD 5	POD 1	Day of drain removal	Length of drain kept (days)	POPF ^a	Postoperative morbidities (Grade) ^b
Case 1	9	5	3	1	1	122	26	5	No	Trocar-site infection (I)
Case 2	10	3	5	2	2	36	21	5	No	No
Case 3	8	5	2	1	1	820	437	7	No	No
Case 4	10	4	3	2	0	190	6	5	No	No
Case 5	8	5	6	2	1	54	11	6	No	No
Case 6	11	5	3	3	2	87	23	5	No	No
Case 7	8	4	2	3	1	120	28	5	No	No
Case 8	14	5	5	3	1	894	382	8	No	No
Case 9	20	5	4	3	1	935	470	9	No	Urinary difficulty (II)
Case 10	18	5	4	2	2	921	395	9	No	Central venous catheter infection (II)
Case 11	18	4	5	3	1	60	15	5	No	Atrial fibrillation (I)
Case 12	17	5	5	3	1	760	210	6	No	No

In this study we considered only Grade B and C postoperative pancreatic fistula (POPF) to be clinically significant according to the International Study Group of Pancreatic Fistula definition.⁸

Postoperative morbidities were classified according to the Clavien–Dindo classification.⁷

POD, postoperative day; VAS, visual analog scale.

These results are comparable or even superior to those in previously published reports on TLPD (Table 3) in terms of the operative time, length of hospital stay, or the estimated blood loss.^2,9–17 The incidence of significant POPF that was Grade B or C ranged from 0% to 27% in previous reports of TLPD, and our study had no case of Grade B or C POPF, although only a small number of cases was included.

Table 3.

Previously Reported Trials or Studies of Total Laparoscopic Pancreaticoduodenectomy

Reference	Number of patients	Year of publication	Operative time (minutes)	EBL (mL)	Length of hospital stay (days)	POPF (%)
Palanivelu et al.¹⁰	42	2007	370	65	10.2	3 (7)
Kendrick and Cusati⁹	62	2010	368	240	7	11 (18)
Zureikat et al.¹²	12	2011	456	300	8	0
Jacobs and Kamyab¹¹	5	2012	589	136	6.6	0
Corcione et al.²	22	2013	392	—	23	6 (27)
Croome et al.¹⁴	108	2014	379	492	6	12 (11)
Speicher et al.¹⁵	25	2014	381	200	8.5	4 (16)
Tan et al.¹⁶	30	2015	513	—	10	1 (3)
Paniccia et al.¹⁷	30	2015	340	300	11	7 (23)
Kim et al. (present study)	12	–	411	118	12.5	0

EBL, estimated blood loss; POPF, postoperative pancreatic fistula.

Discussion

With the recent rapid advancements in laparoscopic techniques and instruments, very specialized pancreatic surgeons have performed TLPD^5,11 since the first case of TLPD was reported in 1994 by Gagner and Pomp.¹⁸ However, only a few cases have been reported, and these studies detail a small number of cases because TLPD is not yet a popular method.^2,13,19 In TLPD, the difficult and fastidious suture motioning is a requisite for the complex anastomosis in a limited space, in contrast to open pancreaticoduodenectomy, which may represent a burden that makes surgeons hesitant to perform TLPD. At our institution Surgeon H began to perform pancreaticoenteric anastomosis using PJt in September 2013 because of its simple properties, which are useful for laparoscopic surgery.

Our PJt method has several advantages that may help surgeons perform LPD more comfortably. The multiple suturing or anchoring of the posterior wall of the pancreas has been the vulnerable point of the surgery due to the laboriousness of intracorporeal suturing. However, with PJt, only two transpancreatic sutures without additional reinforcements are sufficient to complete the anastomosis, and thus this method can reduce the burden on the surgeon to stitch the pancreas wall intracorporeally. Second, in the PJt method, simply passing the needle from the dorsal to the ventral side of the pancreas is sufficient to complete pancreaticoenteric anastomosis via a transpancreatic suture. Only the horizontal force vectors from the dorsal to the ventral side are used, and there is no need to make a difficult suture with an unnatural motion in the vertical direction on the side of the surgeon, such as suturing from the right to the left side of the patient, which can place excessive tangential shear force on the pancreas. Additionally, simply moving the operator's position to the left side of the patient from the right can improve the ergonomics of the second suture at the upper border of the pancreas. In the present analysis, the mean pancreas anastomosis time was 20.1 ± 4.8 minutes, and the mean operative time was 411.6 ± 59.2 minutes. These results are similar to those of previous reports on TLPD. This technique will effectively shorten the anastomosis time and also prevent the unnecessary prolongation of operation time, a disadvantage of LPD. Furthermore, the shortening of the anastomosis time will help reduce operator fatigue, thus enabling more elaborate dissections and manipulations.

A remarkable finding was that we achieved the pancreaticoenteric anastomosis without additional complications such as POPF or bleeding despite the shortened anastomosis time. The technical security of the pancreaticoenteric anastomosis might be more important than its feasibility because anastomosis failure would cause fatal outcomes such as POPF, which can lead to life-threatening complications such as an intraabdominal abscess, peritonitis, sepsis, or even postoperative bleeding. Despite the small number of cases in the current study, our results support PJt in TLPD as a safe method for anastomosis that can avoid significant POPF. We suggest that the characteristics of PJt can explain this result. First, only two transpancreatic sutures are used to complete the anastomosis without reinforcement sutures, and this minimal number of sutures may reduce tissue damage to the pancreas parenchyma and also avoid bleeding caused by pancreas tissue laceration during the penetration of a needle. Second, the use of four buttresses minimizes the gap between the pancreas and jejunal wall and helps make the pancreaticoenteric anastomosis firm. The buttresses provide compressive force to the region around the suture holes and also prevent the squashing of the pancreas parenchyma around the suture sites during tying. Moreover, the buttresses cover the suture holes made as the needle is passed. Potential aperture or stitch holes at the anastomosis site could cause POPF.^20,21 We expect that our PJt using few sutures with buttresses will effectively prevent POPF.

The surgical outcomes described in the present article have inevitable limitations due to the small number of cases. We described our experience with TLPD using PJt and did not compare this method with conventional open pancreaticoduodenectomy. However, as described above, the surgical outcomes of our method suggest that it is feasible and easy to perform in TLPD, as indicated by the estimated blood loss results and the shortened anastomosis time without additional complications. We thus believe that PJt is a useful technique for pancreas anastomosis of TLPD in select patients, particularly due to its simplicity and technical ease in addition to the advantages of minimally invasive surgery. In the near future a comparative study with a large sample size of conventional open pancreaticoduodenectomy and TLPD using other techniques should be performed to estimate the feasibility or superiority of the PJt technique in TLPD.

In conclusion, our novel technique of pancreaticojejunostomy with two transpancreatic sutures with buttresses is a simple, easy, and feasible method for TLPD with the possibility of reducing the burden to the operator and acquiring secure anastomosis.

Footnotes

Disclosure Statement

No competing financial interests exist.

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