J Hepatobiliary Pancreat Sci (2015) 22:202–210 DOI: 10.1002/jhbp.193
REVIEW ARTICLE
Laparoscopic pancreatic reconstruction technique following laparoscopic pancreaticoduodenectomy Chang Moo Kang · Sung Hwan Lee · Myung Jae Chung · Ho Kyoung Hwang · Woo Jung Lee
Published online: 29 December 2014 © 2014 Japanese Society of Hepato-Biliary-Pancreatic Surgery
Abstract With the advance of laparoscopic experiences and techniques, it is carefully regarded that laparoscopic pancreaticoduodenectomy (lap-PD) is feasible and safe in managing perimapullary pancreatic pathology. Especially, laparoscopic management of remnant pancreas can be a critical step toward completeness of minimally invasive PD. According to available published reports, there is a wide range of technical differences in choosing surgical options in managing remnant pancreas after lap-PD. For the evidence-based surgical approach, it would be ideal to test potential techniques by randomized controlled trials, but, currently, it is thought to be very difficult to expect those clinical trials to be successful because there are still a lack of expert surgeons with sound surgical techniques and experience. In addition, lap-PD is so complicated and technically demanding that many surgeons are still questioning whether this surgical approach could be standardized and popular like laparoscopic cholecystectomy. In general, surgical options are usually chosen based on following question: (1) Is it simple? (2) Is it easy and feasible? (3) Is it secure and safe? (4) Is there any supporting scientific evidence? It would be interesting to estimate which surgical technique would be appropriate in managing remnant pancreas under these considerations. It is hoped that a well standardized multicenter-based randomized control study would be successful to test this fundamental issues based on sound surgical techniques and scientific background. C. M. Kang · S. H. Lee · M. J. Chung · H. K. Hwang · W. J. Lee (*) Department of Hepatobiliary and Pancreatic Surgery, Yonsei University College of Medicine, Ludlow Faculty Research Building #203, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea e-mail: [email protected] C. M. Kang · S. H. Lee · M. J. Chung · H. K. Hwang · W. J. Lee Pancreaticobiliary Cancer Clinic, Yonsei Cancer Center, Institute of Gastroenterology, Severance Hospital, Seoul, Korea
Keywords Laparoscopic · Pancreaticoduodenectomy · Pancreaticogastrostomy · Pancreaticojejunostomy · Robotic Introduction Since the first laparoscopic distal pancreatectomy (lap-DP) was reported in the early 1990s [1], accumulating evidence and experience strongly indicate that lap-DP with or without splenectomy is a safe and effective treatment in benign and borderline malignant pancreatic lesions [2–4]. However, controversial issues remain regarding the generalization of laparoscopic pancreaticoduodenectomy (lap-PD). In general, lap-PD may be difficult to perform as a routine procedure. Unlike lap-DP, lap-PD consists of two stages: resection and reconstruction. Both phases are equally important to ensure a safe lap-PD. When dealing with most pancreatic head cancers and some other periampullary cancers, laparoscopic reconstruction can be easy because of secondary dilatation of the bile duct and pancreatic duct in a hardened pancreas; however, laparoscopic resection of the duodenopancreas unit may not be that easy because of inflammatory adhesion to major vascular structures resulted from obstructive cholangitis, pancreatitis, and even direct tumor invasion. In contrast, when treating benign and borderline malignant tumors of the pancreatic head, laparoscopic resection can seem easy, but laparoscopic reconstruction requires a high level of expertise because the lumen of the common bile duct is not usually dilated and the remnant pancreas is soft with a small pancreatic duct (Table 1). Taking it into consideration that a postoperative pancreatic fistula (POPF) is an important source of morbidity in pancreatic surgery, this condition (soft pancreas with small pancreatic duct) has been identified as a critical factor for developing POPF [5, 6] and is regarded as the Achilles Heel in pancreatic surgery. Despite advancements in
J Hepatobiliary Pancreat Sci (2015) 22:202–210
203
Table 1 Surgical concerns in laparoscopic pancreaticoduodenectomy
Jaundice Main pancreatic duct invasion Bile duct dilatation Pancreatic duct Pancreatic texture Inflammatory adhesion (pancreatitis/cholangitis) PV-SMV combined resection Dissection for resection Biliary reconstruction Pancreatic reconstruction
Pancreatic cancer
Benign and borderline malignant tumor
Common Yes Yes Large Hard Yes
Almost no No Almost no Small Soft Almost no
Potentially yes Difficult Easy Easy
Almost no Easy Difficult Difficult
PV-SMV portal vein-superior mesenteric vein.
surgical techniques and perioperative management, morbidity related to PD is estimated to range between 40 and 50%, and POPF is reported to be the most common complication [7]. POPF from pancreatic reconstruction following PD remains a significant cause of morbidity and also contributes significantly to prolonged hospitalization and 30-day mortality [8, 9]. Therefore, laparoscopic management of the remnant pancreas following lap-PD is thought to be one of the critical obstacles to the general practice of lap-PD. When the laparoscopic approach becomes generally accepted for treating benign and borderline malignant pancreatic tumors, laparoscopic reconstruction of the remnant pancreas will be the rate limiting factor to achieving safe lap-PD in benign and borderline malignant pancreatic tumors. To compensate for these technical pitfalls, reconstruction of the remnant pancreas is sometimes left for manual reconstruction under mini-laparotomy [10, 11] or a robotic surgical system [12]. Until now, there have been no randomized controlled trials (RCTs) indicating which laparoscopic techniques are better at managing the remnant pancreas following lap-PD. Such a trial is promising, but it may currently be impossible because of a lack of eligible expert surgeons for lap-PD and the associated technical difficulties. Instead, we may indirectly estimate which surgical technique would be practically feasible via worldwide experts’ experiences. This will be beneficial in reproducing safe surgical performances in the laparoscopic management of the remnant pancreas following lap-PD. Methods Current published reports available in the PubMed were reviewed by searching using combinations of keywords,
including “laparoscopic”, “robotic”, “robot-assisted”, “minimally invasive”, “pancreatectomy”, “pancreaticoduodenectomy”, “pancreatoduodenectomy,” and “Whipple procedure”. In addition, the references and related key words in each article were reviewed for additional reliable citations. In this article, we summarize current practices of laparoscopic management of the remnant pancreas following lap-PD by reviewing the published reports with more than five cases of lap-PD since 2005. We also examined important randomized controlled studies that evaluated the surgical techniques for remnant pancreas to provide additional information to determine appropriate surgical approach in laparoscopic reconstruction of remnant pancreas following PD.
Results Evidence for pancreaticogastrostomy vs. pancreaticojejunostomy It is still under debate which surgical technique for pancreatic anastomosis is best. Some retrospective observational studies suggested that pancreaticogastrostomy (PG) resulted in favorable outcomes in terms of POPF [13–17]. When reviewing a meta-analysis of randomized controlled trials testing PG and pancreaticojejunostomy (PJ) [18, 19], most study suggested that perioperative outcomes such as postoperative morbidity, pancreatic fistula, biliary fistula, reoperation, and hospital stay were not significantly different between the PG and PJ groups (Table 2). Especially, Fernandez-Cruz et al. [22] demonstrated that PG was associated with a lower incidence of POPF than PJ (4% vs. 22%, P < 0.01); however, the surgical technique for PG requires gastric partitioning, which is a complicated procedure that might not always be possible for oncological reasons, especially in laparoscopic situations. There are recent consecutive RCTs proving PG is better in terms with POPF. Figueras et al. [24] investigated the hypothesis that PG would be effective in lowering the incidence and severity of POPF. They found that lower rate of POPF (P = 0.014), less severity of POPF (P = 0.006), and lower incidence of hospital readmission (P = 0.005) were found in the PG group. In addition, Topal et al. [23] also performed a nation-wide multicenter RCT comparing PJ with PG. Although the overall postoperative complication rate was not significantly different between the groups, the clinical postoperative pancreatic fistula rate was much lower in the PG group (8% vs. 19.8%, P = 0.002). They briefly described surgical procedures for PG and PJ (“end-to-side telescoped fashion either into the jejunum or the posterior wall of the stomach”), but did not include detailed descriptions of the surgical procedures. In addition, they omitted
204
J Hepatobiliary Pancreat Sci (2015) 22:202–210
Table 2 Randomized controlled trials testing PG and PJ Author
Year
Cases number (PG/PJ)
Postoperative morbidity (%)
POPF (%)
BF (%)
LOH (day)
Mortality (%)
Reoperation (%)
Yeo et al. [20] Duffas et al. [21] Fernandez-Cruz et al. [22] Topal et al. [23]
1995 2005 2008 2013
73/72 81/68 53/55 162/167
49/43 46/47 23/44 61.7/59.3
12/11 16/21 4/18 8.0/19.8
1/4 7/3 0/2 NA
17.1/17.7 20/21 12/16 19/18
0/0 12/10 0/0 3/5
6/7 19/22 2/2 9/10
BF biliary fistula, LOH length of hospital stay, PG pancreaticogastrostomy, PJ pancreaticojejunostomy, POPF postoperative pancreatic fistula
specific explanations about the number of surgeons involved, how many patients were enrolled per surgeon, the degree of expertise in respect to pancreatic anastomosis, and how they standardized their surgical procedures, all of which suggests a suspiciously wide range of variations (surgeons’ bias) between surgical techniques. Consequently, it is interesting to note that recent meta-analysis of updated RCTs comparing PG and PJ reports that PG provides benefit over PJ after PD, and PG is recommended as a safe and reasonable alternative to PJ in managing remnant pancreas following PD [25, 26]. Dramatic improvement in perioperative mortality and morbidity after PD lead to an expansion of operative indication even to benign and borderline malignant tumors allowing observation of long-term outcome of remnant pancreas after PD. It was reported that cumulative probability of PJ stricture at 1 year was 2.8% (range 0.0–5.9%) and at 5 years was 4.6% (range 0.0–9.2%) among the patients who underwent PD for a benign diagnosis [27]. Especially, as for remnant pancreatic function; several conflicting results are reported about PJ and PG (Table 3). Most series are based on retrospective study design with small sample size. However, recent randomized control study [24] demonstrated that PG can be preferable to PJ by showing PG is related to small amount of body weight change and better exocrine pancreatic function after PD. This debating issue is expected to be further investigated based on well-designed and high powered RCTs in the near future. Evidence for pancreaticojejunostomy: duct-to-mucosa vs. end-to-side invagination technique There have been four randomized trials evaluating a duct-tomucosa versus an end-to-side PJ. A recent meta-analysis [18, 19] showed there were no statistical differences in POPF, postoperative complications, mortality or reoperation between the two groups (Table 4). In particular, the incidence of POPF was not significantly different, even in patients with a soft remnant pancreas (24%, 27 out of 112 patients with duct-to-mucosa PJ, vs. 16%, 20 of 123 patients in end-to-side PJ, OR 1.45 (95% CI, 0.45–4.69), P = 0.54) [18].
Langrehr et al. [35] performed a prospective randomized comparative study between a modified technique for endto-side PJ and a duct-to-mucosa PJ (Cattell technique). The new mattress technique for side-to-side PJ was performed by positioning U-stitches, starting at the jejunal back wall and going from back to front, straight through the pancreatic remnant about 1 cm distal from the cut surface. Next, the sutures were placed through the front wall of the jejunal loop. They reported that the new mattress technique was significantly shorter (15 vs. 22 min., P < 0.0001) and that there were similar postoperative complication rates and length of hospital stay between the two groups; however, a trend toward more reoperations was noted in the Cattell group, with marginal significance (10 vs. 5; P = 0.097). Peng et al. [37] introduced an interesting approach to managing the remnant pancreas following PD. In their prospective randomized trials, they compared a binding technique for PJ (end-to-end, invagination with binding ligature) with conventional PJ (end-to-end, two layered suture technique). It was observed that the incidence of POPF (0 in 106 patients vs. eight out of 111 patients, P = 0.014), overall postoperative complications (24.5% vs. 36.9%, P = 0.048), and length of hospital stay (22.4 days vs.18.4 days, P < 0.001) were significantly superior in the binding PJ group. Future prospective randomized control trials comparing this binding PJ technique with other conventional techniques such as duct-to-mucosa or end-to-side invagination PJ need to be conducted for further investigation. Accordingly, a systemic meta-analysis and randomized controlled trials definitively show there is no one plausible technique for pancreatic reconstruction following PD. The optimal pancreatic anastomosis technique is still up for debate. The safe and appropriate management of the remnant pancreas after PD may depend on meticulous surgical technique, experience, and successful perioperative management rather than the specific type of surgical technique used. It is not clear if this conclusion can be successfully translated into the laparoscopic area; however, considering current advanced laparoscopic techniques and comparable perioperative outcomes in lap-PD [38], it may be feasible even in laparoscopic pancreatic surgery.
J Hepatobiliary Pancreat Sci (2015) 22:202–210
205
Table 3 Studies evaluating remnant pancreatic function after PD between PG and PJ Authors
Study design
Year
PG/PJ
Observation
Conclusion
Morera-Ocon et al. [28]
Retrospective
2014
76/32
• Fecal elastase (μg/g): 61.1 ± 116.4 vs. 50.20 ± 68.5, P = 0.622
Figueras et al. [24]
RCT
2013
65/58
Kim et al. [29]
Retrospective
2009
43/100
Tomimaru et al. [30]
Retrospective
2009
14/28
• Fecal elastase (μg/g): 44 (2–581) vs. 14 (0–190), P = 0.022 • Weight loss (%) –4.5 (–22–4.5) vs. −7 (–25–5), P = 0.025 • Difference in HbA1c level –0.3 vs. −0.1, P = 0.528 • De novo diabetes 7 (11%) vs. 4 (7%), P = 0.443 • Duct size dilatation after 2 years (mm): 4.15 ± 2.48 vs. 3.87 ± 3.53, P > 0.05 • Pancreas thickness after 2 years (mm): 8.19 ± 4.7 vs. 9.3 ± 4.0, P > 0.05 • Steatohrrea: 2 vs. 1, P > 0.05 • New onset DM; 0 vs. 2 • Postoperative albumin: 3.6 ± 0.5 3.7 ± 0.5, P > 0.05 • Postoperative protein: 6.8 ± 0.8 6.7 ± 0.6, P > 0.05 • Postoperative cholesterol: 6.8 ± 0.8 6.7 ± 0.6, P > 0.05 • MPD reduction rate %: −41.653.9 vs. 5.148.3, P = 0.007 • Parenchymal thickness reduction rate, %: 46.025.9 vs 22.419.1, P = 0.0018 • Functional assessment, NA
[Favoring PG] Pancreatic functional concerns about PG cannot reject the hypothesis suggesting PG is useful as elective method for managing remnant soft pancreas. [Favoring PG] PG is associated with low change of weight loss and better exocrine function.
Fang et al. [31]
Retrospective
2007
19/23
Jang et al. [32]
Retrospective
2002
14/20
• Steatorrhea: 12 (63.2%) vs. 10 (43.8%), P > 0.05 • New onset DM: 2 (10.5%) vs. 3 (13%), P > 0.05 HbA1c (%): 6.5 ± 1.5 vs. 6.3 ± 1.1 • Pancreatic duct diameter (mm) Preop: 2.9 ± 3.1 vs. 2.1 T 1.9 Postop: 3.8 T 3.3 ± 3.4 T 2.4, P > 0.05 • Postop albumin: 4.4 ± 0.3 vs. 4.4 ± 0.3, P > 0.05 • Postop protein: 7.6 ± 0.6 vs. 7.6 ± 0.3, P > 0.05 • Postop cholesterol 149.6 ± 31.7 vs. 166.3 ± 29.6, P > 0.05 • Postop triglyceride 130.5 ± 67.0 vs. 124.9 ± 0.76.1, > 0.05 • ≥ 95% body weight recovery rate: 5 (35.7%) vs. 10 (50%), P = 0.266 • Steatorrhea: 9 (64.3%) vs. 3 (15%), P = 0.003 • Stool elastase (μg/g): 12.7 vs. 50.4, P = NA • Stool elastase No Two-layer, interrupted
PJ PJ, modified side-to-side, duct-to-mucosa PG
One-layer, continuous
Two-layer, interrupted
Two-layered, continuous
Two-layer, interrupted
Two-layer, interrupted
NA
NA
NA
NA
89 ± 49
300
74 (35–410)
394 (80–1500)
295 ± 52
360
357 (270–650)
421 (240–660)
368 (258–608)
456 ± 109.5
300 ± 225
240 (30–1200)
568 (536–629)
476
491.5 ± 94
487.3 ± 121.9
597 (420–960)
392 (327–570)
350 (150–625)
485
247 (50–889)
Transfusion, 31 (31%)
220 (150–400)
NA
541 ± 88
473.75 ± 88.27
Operative time (min)
NA
PPH
1 (9.1)
DGE
0 2
4
2 1
1
NA NA
NA
4 (9.5) 3 (7.3%) 5 (9.5) > grade A > grade A
1 (9.1)
POPF (n, %)
0 2
0
0
BF
16 ± 28
NA
8.2 (6–42)
22 (5–85)
7 (4–69)
8 ± 8.5
10 (8–13)
9.79
13.7 ± 6.1
15 ± 9.7
2
2 (10)
5 (5)
1
NA
5
4
15
11 (18)
1
Yes
NA
2
0, > grade A 2
6 (12), 4 (8) >grade A
2
7 (35)
6 (6)
1
NA
NA
NA
9 (15)
3
5
1
1 (5)
2 (2)
NA
NA
2
NA
NA
NA
NA
0
NA
WI
0
NA
NA
NA NA
NA
NA
Yes
1
NA
NA
MS
8
NA
NA
NA
NA
NA
4 (6)
1
4 (8)
2
1 (5)
2 (2)
NA
NA NA
NA
1
0
1 (1.3)
3 (5)
1 (1.6)
1 (7)
1 (2)
1
0
1
0
1
3
NA
3
4 (2.9)
3
1
3
3
2
1
3
2
0
Mortality Reoperation
10 (18.9) 6 (11.3) 3 (5.7)
0
IAA
3 (15) 2 (10)
3 (3)
0 1 0 23 (10–86) 4 > grade A 2 grade > A 1 > grade A 0
8 ± 3.2
18.14 ± 5.99
LOH (day)
BF biliary fistula, DGE delayed gastric emptying, IAA intraabdominal abscess, LOH length of hospital stay, POPF postoperative pancreatic fistula, PPH postpancreatectomy hemorrhage, WI wound infection.
Palanivelu et al. [51] Gumbs et al. [52] Dulucq et al. [53]
Blood loss (ml)
One-layer, 1106 ± 52.67 interrupted, binding ligature Two-layer, 195 ± 136 interrupted
Suture type
NA
Yes
NA
Yes (43)
Yes
Yes
NA
NA
NA
39
1/10
Stent (no/yes)
PG
PJ duct-to-mucosa
PJ duct-to-mucosa
2012 50 (N/A)
Giulianotti 2010 60 (10.4) et al. [50]
Nguyen et al. [47] Zureikat et al. [67] Kendrick et al. [49]
Pancreatic duct occlusion (cyanoacrylate) PG PJ end-to-side, invagination PJ duct-to-mucosa PJ end-to-side, invagination /PJ duct-to-mucosa PJ end-to-side, invagination, small p-duct/PJ duct-to-mucosa, large p-duct PJ end-to-side, invagination, small p-duct (≤3 mm)/PJ duct-to-mucosa, large p-duct (>3 mm) PJ duct-to-mucosa
PJ duct-to-mucosa
PJ sleeve reconstruction, end-to-end
Technique
R* lap resection+ robot reconstruction R
R
L
2013 90 (4.8)
2012 20 (5)
R
L
L
3 (9.1) 2013 34 (0)
3 10
Chalikonda 2012 30 (10) et al. [46]
Lai et al. [45]
Boggi et al. [43] Kim et al. [44]
2012 41 (16.9)
Asbun et al. [38]
6
2013 11 (NA)
Lei et al. [41]
L
Year Patients Surgical number approach (conversion rate, %)
Authors
Table 5 Summary of the literature reporting laparoscopic pancreaticoduodenectomy
Intestinal obstruction (1), gastroduodenal stenosis (1), tube-gastrostomy
POPF (1), biliary fistula (1), A-loop obstruction (1)
Peritonitis after PG (1), wound debridement (1), esophageal rupture (1), massive colonic ischemia (1)
POPF (1), bleeding (1), biliary fistula (1)
Gastric staple line bleeding (1)
POPF (2), intestinal obstruction (1)
POPF (2), wound dehiscence (1)
Bleeding from POPF (1), ischemic colon (1)
Bleeding (1)
Bleeding (3)
Bleeding and jejunal stump leakage (1), afferent loop obstruction (1)
J Hepatobiliary Pancreat Sci (2015) 22:202–210 207
208
by a backhanded stitch technique with the Haenawa. Ductto-mucosa anastomosis or an internal drainage technique was used for inner layer anastomosis, and in the case of a soft pancreas with a small pancreatic duct, a short stent tube was inserted into the small jejunal orifice after fixation to the main pancreatic duct. After managing the inner layer, serial approximations of Haenawa sutures can be used to complete PJ. It was reported that among 17 patients who underwent laparoscopic PJ with the Haenawa technique, two patients developed clinically relevant POPF, which was managed with conservative measures. Nakamura et al. [11] described another reliable PJ method with closure of the pancreatic stump by an endoscopic linear stapler in lap-PD. This reconstruction technique is a manual reconstruction through a small external wound. The remaining staples ligating the main pancreatic duct were removed to open the main pancreatic duct, and the stent tube was inserted for manual duct-to-mucosa PJ. Additional staples in the pancreatic parenchyma outside the main pancreatic duct were left in place in order to prevent leakage of pancreatic juice from the branches of the pancreatic duct. This technique is modified from a previous report from the Fundan University group in China [60]. Instead of manual closure of the remnant pancreatic stump in an interrupted fashion by inverting sutures with a stent tube in the main pancreatic duct, Nakamura et al. used a stapler in the laparoscopic environment. It was reported that only one patient (5.9%) experienced POPF among 17 patients with this PJ technique following lap-PD.
Discussion In 1994, Gagner and Pomp [61] reported the first successful lap-PD in a 30-year-old female patient with chronic pancreatitis and demonstrated the technical feasibility of a laparoscopic approach to pancreatic head lesions; however, it was thought that the potential benefit of such a minimally invasive surgery may not be as apparent as that of a more common less complex surgical procedure because of technical complexity and potential postoperative high morbidity. Several other clinical series reporting surgical experiences of lap-PD reached similar conclusions [62–64]. Since then, lap-PD was regarded as a myth in the laparoscopic surgical field. However, in 2007, ground-breaking literature was published by Palanivelu et al. [65] from India, inspiring renewed interest in lap-PD. They reported 42 patients who underwent lap-PD, and more surprisingly, most patients (40 out of 42 patients) had periampullary cancers. They described the surgical techniques, comparable perioperative results, and acceptable long-term oncologic outcomes, suggesting that lap-PD can be performed safely and with good
J Hepatobiliary Pancreat Sci (2015) 22:202–210
surgical results in well-selected patients. After their reports and video presentation were released, many laparoscopic surgeons attempted to perform lap-PD relying on their own accumulated laparoscopic experience, techniques and advanced instruments. As a result, several promising reports have recently been reproduced in highly specialized medical centers [44, 49, 51], and some expert surgeons agree that lap-PD is safe and its perioperative outcomes are comparable to those of an open approach [38, 66]. In general, the following questions are relevant when choosing a surgical technique in daily clinical practice: (1) Is it simple? (2) Is it technically easy and feasible? (3) Is it secure and safe? (4) Is there any supporting scientific evidence? According to a literature review of the current practice of laparoscopic reconstruction techniques for the remnant pancreas following PD, in spite of technical variations, PJ (ductto-mucosa or end-to-side PJ) was found to be the most popular procedure following lap-PD. In an open surgical environment, the clinical evidence suggests that there are no superior surgical options for reconstruction of the remnant pancreas following PD. It may depend on the surgeons’ expertise, experience, the texture of the pancreas, and the patient’s condition. These accumulating data can be used as indirect evidence in choosing a laparoscopic pancreatic reconstruction technique; however, laparoscopic PG may not be appropriate, because of the specific anatomic relationship between the stomach and the remnant pancreas, which makes PG more difficult in laparoscopic circumstances. Laparoscopic PJ (duct-to-mucosa) is technically feasible, but it might be somewhat complicated, and technically very difficult in the case of a soft pancreas with a small pancreatic duct. To the contrary, laparoscopic end-to-side PJ (dunking) method is thought to be another good option in managing the remnant pancreas following lap-PD. It is a relatively simple technique and can be performed even in a soft pancreas with a small pancreatic duct. This surgical technique is strongly supported by a previous randomized controlled study and abundant experiences [58]. However, “appropriate surgical technique” may depend on patients’ conditions, surgeons’ experience/technique, and hospital facility with available perioperative management. Ideally, multicenter randomized controlled trial with strict standardized surgical techniques is required to provide a proper answer to this question, but technically it might be very difficult. Acknowledgments Some part of this manuscript was presented in the Symposium: How to Manage the Remnant Pancreas After Laparoscopic Pancreaticoduodenectomy (8TH International Single Topic Symposium of the Korean Association of HBP surgery, on 13 October 2013, Cheongju, South Korea). The authors would like to express sincere gratitude to their international colleagues; Dr Yoshiharu Nakamura (Nippon Medical School), Dr Akira Matsushita (Nippon
J Hepatobiliary Pancreat Sci (2015) 22:202–210 Medical School), and Yuichi Nagakawa (Tokyo Medical University) for providing their valuable comments, which improved the content of this paper. Conflict of interest
None declared.
References 1. Gagner M, Pomp A, Herrera MF. Early experience with laparoscopic resections of islet cell tumors. Surgery. 1996;120: 1051–4. 2. Jin T, Altaf K, Xiong JJ, Huang W, Javed MA, Mai G, et al. A systematic review and meta-analysis of studies comparing laparoscopic and open distal pancreatectomy. HPB. 2012;14:711–24. 3. Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048–59. 4. Pericleous S, Middleton N, McKay SC, Bowers KA, Hutchins RR. Systematic review and meta-analysis of case-matched studies comparing open and laparoscopic distal pancreatectomy: is it a safe procedure? Pancreas. 2012;41:993–1000. 5. Ramacciato G, Mercantini P, Petrucciani N, Nigri GR, Kazemi A, Muroni M, et al. Risk factors of pancreatic fistula after pancreaticoduodenectomy: a collective review. Am Surg. 2011;77:257– 69. 6. Ball CG, Howard TJ. Does the type of pancreaticojejunostomy after Whipple alter the leak rate? Adv Surg. 2010;44:131–48. 7. 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;10:1199–210. 8. Pratt WB, Maithel SK, Vanounou T, Huang ZS, Callery MP, Vollmer CM, Jr. Clinical and economic validation of the International Study Group of Pancreatic Fistula (ISGPF) classification scheme. Ann Surg. 2007;245:443–51. 9. Buchler MW, Friess H, Wagner M, Kulli C, Wagener V, Z’Graggen K. Pancreatic fistula after pancreatic head resection. Br J Surg. 2000;87:883–9. 10. Lee JS, Han JH, Na GH, Choi HJ, Hong TH, You YK, et al. Laparoscopic pancreaticoduodenectomy assisted by minilaparotomy. Surg Laparosc Endosc Percutan Tech. 2013;23:e98– 102. 11. Nakamura Y, Matsumoto S, Matsushita A, Yoshioka M, Shimizu T, Yamahatsu K, et al. Pancreaticojejunostomy with closure of the pancreatic stump by endoscopic linear stapler in laparoscopic pancreaticoduodenectomy: a reliable technique and benefits for pancreatic resection. Asian J Endosc Surg. 2012;5:191–4. 12. Narula VK, Mikami DJ, Melvin WS. Robotic and laparoscopic pancreaticoduodenectomy: a hybrid approach. Pancreas. 2010;39: 160–4. 13. Kim SW, Youk EG, Park YH. Comparison of pancreatogastrostomy and pancreatojejunostomy after pancreatoduodenectomy performed by one surgeon. World J Surg. 1997;21: 640–3. 14. Takano S, Ito Y, Watanabe Y, Yokoyama T, Kubota N, Iwai S. Pancreaticojejunostomy versus pancreaticogastrostomy in reconstruction following pancreaticoduodenectomy. Br J Surg. 2000;87:423–7. 15. Fujino Y, Suzuki Y, Ajiki T, Tanioka Y, Ku Y, Kuroda Y. Risk factors influencing pancreatic leakage and the mortality after pancreaticoduodenectomy in a medium-volume hospital. Hepatogastroenterology. 2002;49:1124–9.
209
16. Schlitt HJ, Schmidt U, Simunec D, Jager M, Aselmann H, Neipp M, et al. Morbidity and mortality associated with pancreatogastrostomy and pancreatojejunostomy following partial pancreatoduodenectomy. Br J Surg. 2002;89:1245–51. 17. Oussoultzoglou E, Bachellier P, Bigourdan JM, Weber JC, Nakano H, Jaeck D. Pancreaticogastrostomy decreased relaparotomy caused by pancreatic fistula after pancreaticoduodenectomy compared with pancreaticojejunostomy. Arch Surg. 2004;139:327–35. 18. Yang SH, Dou KF, Sharma N, Song WJ. The methods of reconstruction of pancreatic digestive continuity after pancreaticoduodenectomy: a meta-analysis of randomized controlled trials. World J Surg. 2011;35:2290–7. 19. Wente MN, Shrikhande SV, Muller MW, Diener MK, Seiler CM, Friess H, et al. Pancreaticojejunostomy versus pancreaticogastrostomy: systematic review and meta-analysis. Am J Surg. 2007;193:171–83. 20. Yeo CJ, Cameron JL, Maher MM, Sauter PK, Zahurak ML, Talamini MA, et al. A prospective randomized trial of pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy. Ann Surg. 1995;222:580–8; discussion 8–92. 21. Duffas JP, Suc B, Msika S, Fourtanier G, Muscari F, Hay JM, et al. A controlled randomized multicenter trial of pancreatogastrostomy or pancreatojejunostomy after pancreatoduodenectomy. Am J Surg. 2005;189:720–9. 22. Fernandez-Cruz L, Cosa R, Blanco L, Lopez-Boado MA, Astudillo E. Pancreatogastrostomy with gastric partition after pylorus-preserving pancreatoduodenectomy versus conventional pancreatojejunostomy: a prospective randomized study. Ann Surg. 2008;248:930–8. 23. Topal B, Fieuws S, Aerts R, Weerts J, Feryn T, Roeyen G, et al. Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy for pancreatic or periampullary tumours: a multicentre randomised trial. Lancet Oncol. 2013;14:655–62. 24. Figueras J, Sabater L, Planellas P, Muñoz-Forner E, Lopez-Ben S, Falgueras L, et al. Randomized clinical trial of pancreaticogastrostomy versus pancreaticojejunostomy on the rate and severity of pancreatic fistula after pancreaticoduodenectomy. Br J Surg. 2013;100:1597–605. 25. Menahem B, Guittet L, Mulliri A, Alves A, Lubrano J. Pancreaticogastrostomy is superior to pancreaticojejunostomy for prevention of pancreatic fistula after pancreaticoduodenectomy: an updated meta-analysis of randomized controlled trials. Ann Surg. 2014; doi: 10.1097/SLA.0000000000000806. 26. Liu FB, Chen JM, Geng W, Xie SX, Zhao YJ, Yu LQ, et al. Pancreaticogastrostomy is associated with significantly less pancreatic fistula than pancreaticojejunostomy reconstruction after pancreaticoduodenectomy: a meta-analysis of seven randomized controlled trials. HPB (Oxford). 2014; doi: 10.1111/hpb.12279. 27. Reid-Lombardo KM, Ramos-De la Medina A, Thomsen K, Harmsen WS, Farnell MB. Long-term anastomotic complications after pancreaticoduodenectomy for benign diseases. J Gastrointest Surg. 2007;11:1704–11. 28. Morera-Ocon FJ, Sabater-Orti L, Munoz-Forner E, Perez-Griera J, Ortega-Serrano J. Considerations on pancreatic exocrine function after pancreaticoduodenectomy. World J Gastrointest Oncol. 2014;6:325–9. 29. Kim JH, Yoo BM, Kim JH, Kim WH. Which method should we select for pancreatic anastomosis after pancreaticoduodenectomy? World J Surg. 2009;33:326–32. 30. Tomimaru Y, Takeda Y, Kobayashi S, Marubashi S, Lee CM, Tanemura M, et al. Comparison of postoperative morphological changes in remnant pancreas between pancreaticojejunostomy and pancreaticogastrostomy after pancreaticoduodenectomy. Pancreas. 2009;38:203–7.
210 31. Fang WL, Su CH, Shyr YM, Chen TH, Lee RC, Tai LC, et al. Functional and morphological changes in pancreatic remnant after pancreaticoduodenectomy. Pancreas. 2007;35:361–5. 32. Jang JY, Kim SW, Park SJ, Park YH. Comparison of the functional outcome after pylorus-preserving pancreatoduodenectomy: pancreatogastrostomy and pancreatojejunostomy. World J Surg. 2002;26:366–71. 33. Chou FF, Sheen-Chen SM, Chen YS, Chen MC, Chen CL. Postoperative morbidity and mortality of pancreaticoduodenectomy for periampullary cancer. Eur J Surg. 1996;162:477–81. 34. 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– 71. 35. Langrehr JM, Bahra M, Jacob D, Glanemann M, Neuhaus P. Prospective randomized comparison between a new mattress technique and Cattell (duct-to-mucosa) pancreaticojejunostomy for pancreatic resection. World J Surg. 2005;29:1111–19; discussion 20-1. 36. 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;208:738–47. 37. 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;245:692–8. 38. Asbun HJ, Stauffer JA. Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J Am Coll Surg. 2012;215:810–19. 39. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, et al. Comparison of laparoscopy-assisted and open pylorus-preserving pancreaticoduodenectomy for periampullary disease. Am J Surg. 2009;198:445–9. 40. Choi SH, Kang CM, Kim DH, Lee WJ, Chi HS. Robotic pylorus preserving pancreaticoduodenectomy with mini-laparotomy reconstruction in patient with ampullary adenoma. J Korean Surg Soc. 2011;81:355–9. 41. Lei Z, Zhifei W, Jun X, Chang L, Lishan X, Yinghui G, et al. Pancreaticojejunostomy sleeve reconstruction after pancreaticoduodenectomy in laparoscopic and open surgery. JSLS. 2013; 17:68–73. 42. Corcione F, Pirozzi F, Cuccurullo D, Piccolboni D, Caracino V, Galante F, et al. Laparoscopic pancreaticoduodenectomy: experience of 22 cases. Surg Endosc. 2013;27:2131–6. 43. Boggi U, Signori S, De Lio N, Perrone VG, Vistoli F, Belluomini M, et al. Feasibility of robotic pancreaticoduodenectomy. Br J Surg. 2013;100:917–25. 44. Kim SC, Song KB, Jung YS, Kim YH, Park do H, Lee SS, et al. Short-term clinical outcomes for 100 consecutive cases of laparoscopic pylorus-preserving pancreatoduodenectomy: improvement with surgical experience. Surg Endosc. 2013;27:95–103. 45. Lai EC, Yang GP, Tang CN. Robot-assisted laparoscopic pancreaticoduodenectomy versus open pancreaticoduodenectomy —a comparative study. Int J Surg. 2012;10:475–9. 46. Chalikonda S, Aguilar-Saavedra JR, Walsh RM. Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg Endosc. 2012;26:2397–402. 47. Nguyen KT, Zureikat AH, Chalikonda S, Bartlett DL, Moser AJ, Zeh HJ. Technical aspects of robotic-assisted pancreaticoduodenectomy (RAPD). J Gastrointest Surg. 2011;15:870–5.
J Hepatobiliary Pancreat Sci (2015) 22:202–210 48. Abood GJ, Can MF, Daouadi M, Huss HT, Steve JY, Ramalingam L, et al. Robotic-assisted minimally invasive central pancreatectomy: technique and outcomes. J Gastrointest Surg. 2013;17: 1002–8. 49. Kendrick ML, Cusati D. Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg. 2010;145:19–23. 50. Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P, et al. Robot-assisted laparoscopic pancreatic surgery: singlesurgeon experience. Surg Endosc. 2010;24:1646–57. 51. Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, et al. Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg. 2009; 16:731–40. 52. Gumbs AA, Gres P, Madureira FA, Gayet B. Laparoscopic vs. open resection of noninvasive intraductal pancreatic mucinous neoplasms. J Gastrointest Surg. 2008;12:707–12. 53. Dulucq JL, Wintringer P, Mahajna A. Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surg Endosc. 2006;20:1045–50. 54. Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, et al. Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg. 2000;4:567–79. 55. Schnelldorfer T, Ware AL, Sarr MG, Smyrk TC, Zhang L, Qin R, et al. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible? Ann Surg. 2008;247: 456–62. 56. Kang CM, Kim DH, Lee WJ, Chi HS. Initial experiences using robot-assisted central pancreatectomy with pancreaticogastrostomy: a potential way to advanced laparoscopic pancreatectomy. Surg Endosc. 2011;25:1101–6. 57. Giulianotti PC, Sbrana F, Bianco FM, Addeo P, Caravaglios G. Robot-assisted laparoscopic middle pancreatectomy. J Laparoendosc Adv Surg Tech A. 2010;20:135–9. 58. Eugene P, Kennedy CJY. Dunking pancreaticojejunostomy versus duct-to-mucosa anastomosis. J Hepatobiliary Pancreat Sci. 2011; 18:769–74. 59. Honda G, Kurata M, Okuda Y, Kobayashi S, Yamaguchi T, Matsumoto H, et al. Novel device for pancreaticojejunostomy via a pure laparoscopic approach. J Am Coll Surg. 2013;216:e73–6. 60. Liu C, Long J, Liu L, Xu J, Zhang B, Yu X, et al. Pancreatic stump-closed pancreaticojejunostomy can be performed safely in normal soft pancreas cases. J Surg Res. 2012;172:e11–7. 61. Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc. 1994;8:408–10. 62. Cuschieri A. Laparoscopic pancreatic resections. Semin Laparosc Surg. 1996;3:15–20. 63. Park A, Schwartz R, Tandan V, Anvari M. Laparoscopic pancreatic surgery. Am J Surg. 1999;177:158–63. 64. Underwood RA, Soper NJ. Current status of laparoscopic surgery of the pancreas. J Hepatobiliary Pancreat Surg. 1999;6:154–64. 65. Palanivelu C, Jani K, Senthilnathan P, Parthasarathi R, Rajapandian S, Madhankumar MV. Laparoscopic pancreaticoduodenectomy: technique and outcomes. J Am Coll Surg. 2007; 205:222–30. 66. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, et al. Laparoscopic major hepato-biliary-pancreatic surgery: formidable challenge to standardization. J Hepatobiliary Pancreat Surg. 2009;16:705–10. 67. Zureikat AH, Breaux JA, Steel JL, Hughes SJ. Can laparoscopic pancreaticoduodenectomy be safely implemented? J Gastrointest Surg. 2011;15:1151–7.
REVIEW ARTICLE
Laparoscopic pancreatic reconstruction technique following laparoscopic pancreaticoduodenectomy Chang Moo Kang · Sung Hwan Lee · Myung Jae Chung · Ho Kyoung Hwang · Woo Jung Lee
Published online: 29 December 2014 © 2014 Japanese Society of Hepato-Biliary-Pancreatic Surgery
Abstract With the advance of laparoscopic experiences and techniques, it is carefully regarded that laparoscopic pancreaticoduodenectomy (lap-PD) is feasible and safe in managing perimapullary pancreatic pathology. Especially, laparoscopic management of remnant pancreas can be a critical step toward completeness of minimally invasive PD. According to available published reports, there is a wide range of technical differences in choosing surgical options in managing remnant pancreas after lap-PD. For the evidence-based surgical approach, it would be ideal to test potential techniques by randomized controlled trials, but, currently, it is thought to be very difficult to expect those clinical trials to be successful because there are still a lack of expert surgeons with sound surgical techniques and experience. In addition, lap-PD is so complicated and technically demanding that many surgeons are still questioning whether this surgical approach could be standardized and popular like laparoscopic cholecystectomy. In general, surgical options are usually chosen based on following question: (1) Is it simple? (2) Is it easy and feasible? (3) Is it secure and safe? (4) Is there any supporting scientific evidence? It would be interesting to estimate which surgical technique would be appropriate in managing remnant pancreas under these considerations. It is hoped that a well standardized multicenter-based randomized control study would be successful to test this fundamental issues based on sound surgical techniques and scientific background. C. M. Kang · S. H. Lee · M. J. Chung · H. K. Hwang · W. J. Lee (*) Department of Hepatobiliary and Pancreatic Surgery, Yonsei University College of Medicine, Ludlow Faculty Research Building #203, 50 Yonsei-ro, Seodaemun-gu, Seoul 120-752, Korea e-mail: [email protected] C. M. Kang · S. H. Lee · M. J. Chung · H. K. Hwang · W. J. Lee Pancreaticobiliary Cancer Clinic, Yonsei Cancer Center, Institute of Gastroenterology, Severance Hospital, Seoul, Korea
Keywords Laparoscopic · Pancreaticoduodenectomy · Pancreaticogastrostomy · Pancreaticojejunostomy · Robotic Introduction Since the first laparoscopic distal pancreatectomy (lap-DP) was reported in the early 1990s [1], accumulating evidence and experience strongly indicate that lap-DP with or without splenectomy is a safe and effective treatment in benign and borderline malignant pancreatic lesions [2–4]. However, controversial issues remain regarding the generalization of laparoscopic pancreaticoduodenectomy (lap-PD). In general, lap-PD may be difficult to perform as a routine procedure. Unlike lap-DP, lap-PD consists of two stages: resection and reconstruction. Both phases are equally important to ensure a safe lap-PD. When dealing with most pancreatic head cancers and some other periampullary cancers, laparoscopic reconstruction can be easy because of secondary dilatation of the bile duct and pancreatic duct in a hardened pancreas; however, laparoscopic resection of the duodenopancreas unit may not be that easy because of inflammatory adhesion to major vascular structures resulted from obstructive cholangitis, pancreatitis, and even direct tumor invasion. In contrast, when treating benign and borderline malignant tumors of the pancreatic head, laparoscopic resection can seem easy, but laparoscopic reconstruction requires a high level of expertise because the lumen of the common bile duct is not usually dilated and the remnant pancreas is soft with a small pancreatic duct (Table 1). Taking it into consideration that a postoperative pancreatic fistula (POPF) is an important source of morbidity in pancreatic surgery, this condition (soft pancreas with small pancreatic duct) has been identified as a critical factor for developing POPF [5, 6] and is regarded as the Achilles Heel in pancreatic surgery. Despite advancements in
J Hepatobiliary Pancreat Sci (2015) 22:202–210
203
Table 1 Surgical concerns in laparoscopic pancreaticoduodenectomy
Jaundice Main pancreatic duct invasion Bile duct dilatation Pancreatic duct Pancreatic texture Inflammatory adhesion (pancreatitis/cholangitis) PV-SMV combined resection Dissection for resection Biliary reconstruction Pancreatic reconstruction
Pancreatic cancer
Benign and borderline malignant tumor
Common Yes Yes Large Hard Yes
Almost no No Almost no Small Soft Almost no
Potentially yes Difficult Easy Easy
Almost no Easy Difficult Difficult
PV-SMV portal vein-superior mesenteric vein.
surgical techniques and perioperative management, morbidity related to PD is estimated to range between 40 and 50%, and POPF is reported to be the most common complication [7]. POPF from pancreatic reconstruction following PD remains a significant cause of morbidity and also contributes significantly to prolonged hospitalization and 30-day mortality [8, 9]. Therefore, laparoscopic management of the remnant pancreas following lap-PD is thought to be one of the critical obstacles to the general practice of lap-PD. When the laparoscopic approach becomes generally accepted for treating benign and borderline malignant pancreatic tumors, laparoscopic reconstruction of the remnant pancreas will be the rate limiting factor to achieving safe lap-PD in benign and borderline malignant pancreatic tumors. To compensate for these technical pitfalls, reconstruction of the remnant pancreas is sometimes left for manual reconstruction under mini-laparotomy [10, 11] or a robotic surgical system [12]. Until now, there have been no randomized controlled trials (RCTs) indicating which laparoscopic techniques are better at managing the remnant pancreas following lap-PD. Such a trial is promising, but it may currently be impossible because of a lack of eligible expert surgeons for lap-PD and the associated technical difficulties. Instead, we may indirectly estimate which surgical technique would be practically feasible via worldwide experts’ experiences. This will be beneficial in reproducing safe surgical performances in the laparoscopic management of the remnant pancreas following lap-PD. Methods Current published reports available in the PubMed were reviewed by searching using combinations of keywords,
including “laparoscopic”, “robotic”, “robot-assisted”, “minimally invasive”, “pancreatectomy”, “pancreaticoduodenectomy”, “pancreatoduodenectomy,” and “Whipple procedure”. In addition, the references and related key words in each article were reviewed for additional reliable citations. In this article, we summarize current practices of laparoscopic management of the remnant pancreas following lap-PD by reviewing the published reports with more than five cases of lap-PD since 2005. We also examined important randomized controlled studies that evaluated the surgical techniques for remnant pancreas to provide additional information to determine appropriate surgical approach in laparoscopic reconstruction of remnant pancreas following PD.
Results Evidence for pancreaticogastrostomy vs. pancreaticojejunostomy It is still under debate which surgical technique for pancreatic anastomosis is best. Some retrospective observational studies suggested that pancreaticogastrostomy (PG) resulted in favorable outcomes in terms of POPF [13–17]. When reviewing a meta-analysis of randomized controlled trials testing PG and pancreaticojejunostomy (PJ) [18, 19], most study suggested that perioperative outcomes such as postoperative morbidity, pancreatic fistula, biliary fistula, reoperation, and hospital stay were not significantly different between the PG and PJ groups (Table 2). Especially, Fernandez-Cruz et al. [22] demonstrated that PG was associated with a lower incidence of POPF than PJ (4% vs. 22%, P < 0.01); however, the surgical technique for PG requires gastric partitioning, which is a complicated procedure that might not always be possible for oncological reasons, especially in laparoscopic situations. There are recent consecutive RCTs proving PG is better in terms with POPF. Figueras et al. [24] investigated the hypothesis that PG would be effective in lowering the incidence and severity of POPF. They found that lower rate of POPF (P = 0.014), less severity of POPF (P = 0.006), and lower incidence of hospital readmission (P = 0.005) were found in the PG group. In addition, Topal et al. [23] also performed a nation-wide multicenter RCT comparing PJ with PG. Although the overall postoperative complication rate was not significantly different between the groups, the clinical postoperative pancreatic fistula rate was much lower in the PG group (8% vs. 19.8%, P = 0.002). They briefly described surgical procedures for PG and PJ (“end-to-side telescoped fashion either into the jejunum or the posterior wall of the stomach”), but did not include detailed descriptions of the surgical procedures. In addition, they omitted
204
J Hepatobiliary Pancreat Sci (2015) 22:202–210
Table 2 Randomized controlled trials testing PG and PJ Author
Year
Cases number (PG/PJ)
Postoperative morbidity (%)
POPF (%)
BF (%)
LOH (day)
Mortality (%)
Reoperation (%)
Yeo et al. [20] Duffas et al. [21] Fernandez-Cruz et al. [22] Topal et al. [23]
1995 2005 2008 2013
73/72 81/68 53/55 162/167
49/43 46/47 23/44 61.7/59.3
12/11 16/21 4/18 8.0/19.8
1/4 7/3 0/2 NA
17.1/17.7 20/21 12/16 19/18
0/0 12/10 0/0 3/5
6/7 19/22 2/2 9/10
BF biliary fistula, LOH length of hospital stay, PG pancreaticogastrostomy, PJ pancreaticojejunostomy, POPF postoperative pancreatic fistula
specific explanations about the number of surgeons involved, how many patients were enrolled per surgeon, the degree of expertise in respect to pancreatic anastomosis, and how they standardized their surgical procedures, all of which suggests a suspiciously wide range of variations (surgeons’ bias) between surgical techniques. Consequently, it is interesting to note that recent meta-analysis of updated RCTs comparing PG and PJ reports that PG provides benefit over PJ after PD, and PG is recommended as a safe and reasonable alternative to PJ in managing remnant pancreas following PD [25, 26]. Dramatic improvement in perioperative mortality and morbidity after PD lead to an expansion of operative indication even to benign and borderline malignant tumors allowing observation of long-term outcome of remnant pancreas after PD. It was reported that cumulative probability of PJ stricture at 1 year was 2.8% (range 0.0–5.9%) and at 5 years was 4.6% (range 0.0–9.2%) among the patients who underwent PD for a benign diagnosis [27]. Especially, as for remnant pancreatic function; several conflicting results are reported about PJ and PG (Table 3). Most series are based on retrospective study design with small sample size. However, recent randomized control study [24] demonstrated that PG can be preferable to PJ by showing PG is related to small amount of body weight change and better exocrine pancreatic function after PD. This debating issue is expected to be further investigated based on well-designed and high powered RCTs in the near future. Evidence for pancreaticojejunostomy: duct-to-mucosa vs. end-to-side invagination technique There have been four randomized trials evaluating a duct-tomucosa versus an end-to-side PJ. A recent meta-analysis [18, 19] showed there were no statistical differences in POPF, postoperative complications, mortality or reoperation between the two groups (Table 4). In particular, the incidence of POPF was not significantly different, even in patients with a soft remnant pancreas (24%, 27 out of 112 patients with duct-to-mucosa PJ, vs. 16%, 20 of 123 patients in end-to-side PJ, OR 1.45 (95% CI, 0.45–4.69), P = 0.54) [18].
Langrehr et al. [35] performed a prospective randomized comparative study between a modified technique for endto-side PJ and a duct-to-mucosa PJ (Cattell technique). The new mattress technique for side-to-side PJ was performed by positioning U-stitches, starting at the jejunal back wall and going from back to front, straight through the pancreatic remnant about 1 cm distal from the cut surface. Next, the sutures were placed through the front wall of the jejunal loop. They reported that the new mattress technique was significantly shorter (15 vs. 22 min., P < 0.0001) and that there were similar postoperative complication rates and length of hospital stay between the two groups; however, a trend toward more reoperations was noted in the Cattell group, with marginal significance (10 vs. 5; P = 0.097). Peng et al. [37] introduced an interesting approach to managing the remnant pancreas following PD. In their prospective randomized trials, they compared a binding technique for PJ (end-to-end, invagination with binding ligature) with conventional PJ (end-to-end, two layered suture technique). It was observed that the incidence of POPF (0 in 106 patients vs. eight out of 111 patients, P = 0.014), overall postoperative complications (24.5% vs. 36.9%, P = 0.048), and length of hospital stay (22.4 days vs.18.4 days, P < 0.001) were significantly superior in the binding PJ group. Future prospective randomized control trials comparing this binding PJ technique with other conventional techniques such as duct-to-mucosa or end-to-side invagination PJ need to be conducted for further investigation. Accordingly, a systemic meta-analysis and randomized controlled trials definitively show there is no one plausible technique for pancreatic reconstruction following PD. The optimal pancreatic anastomosis technique is still up for debate. The safe and appropriate management of the remnant pancreas after PD may depend on meticulous surgical technique, experience, and successful perioperative management rather than the specific type of surgical technique used. It is not clear if this conclusion can be successfully translated into the laparoscopic area; however, considering current advanced laparoscopic techniques and comparable perioperative outcomes in lap-PD [38], it may be feasible even in laparoscopic pancreatic surgery.
J Hepatobiliary Pancreat Sci (2015) 22:202–210
205
Table 3 Studies evaluating remnant pancreatic function after PD between PG and PJ Authors
Study design
Year
PG/PJ
Observation
Conclusion
Morera-Ocon et al. [28]
Retrospective
2014
76/32
• Fecal elastase (μg/g): 61.1 ± 116.4 vs. 50.20 ± 68.5, P = 0.622
Figueras et al. [24]
RCT
2013
65/58
Kim et al. [29]
Retrospective
2009
43/100
Tomimaru et al. [30]
Retrospective
2009
14/28
• Fecal elastase (μg/g): 44 (2–581) vs. 14 (0–190), P = 0.022 • Weight loss (%) –4.5 (–22–4.5) vs. −7 (–25–5), P = 0.025 • Difference in HbA1c level –0.3 vs. −0.1, P = 0.528 • De novo diabetes 7 (11%) vs. 4 (7%), P = 0.443 • Duct size dilatation after 2 years (mm): 4.15 ± 2.48 vs. 3.87 ± 3.53, P > 0.05 • Pancreas thickness after 2 years (mm): 8.19 ± 4.7 vs. 9.3 ± 4.0, P > 0.05 • Steatohrrea: 2 vs. 1, P > 0.05 • New onset DM; 0 vs. 2 • Postoperative albumin: 3.6 ± 0.5 3.7 ± 0.5, P > 0.05 • Postoperative protein: 6.8 ± 0.8 6.7 ± 0.6, P > 0.05 • Postoperative cholesterol: 6.8 ± 0.8 6.7 ± 0.6, P > 0.05 • MPD reduction rate %: −41.653.9 vs. 5.148.3, P = 0.007 • Parenchymal thickness reduction rate, %: 46.025.9 vs 22.419.1, P = 0.0018 • Functional assessment, NA
[Favoring PG] Pancreatic functional concerns about PG cannot reject the hypothesis suggesting PG is useful as elective method for managing remnant soft pancreas. [Favoring PG] PG is associated with low change of weight loss and better exocrine function.
Fang et al. [31]
Retrospective
2007
19/23
Jang et al. [32]
Retrospective
2002
14/20
• Steatorrhea: 12 (63.2%) vs. 10 (43.8%), P > 0.05 • New onset DM: 2 (10.5%) vs. 3 (13%), P > 0.05 HbA1c (%): 6.5 ± 1.5 vs. 6.3 ± 1.1 • Pancreatic duct diameter (mm) Preop: 2.9 ± 3.1 vs. 2.1 T 1.9 Postop: 3.8 T 3.3 ± 3.4 T 2.4, P > 0.05 • Postop albumin: 4.4 ± 0.3 vs. 4.4 ± 0.3, P > 0.05 • Postop protein: 7.6 ± 0.6 vs. 7.6 ± 0.3, P > 0.05 • Postop cholesterol 149.6 ± 31.7 vs. 166.3 ± 29.6, P > 0.05 • Postop triglyceride 130.5 ± 67.0 vs. 124.9 ± 0.76.1, > 0.05 • ≥ 95% body weight recovery rate: 5 (35.7%) vs. 10 (50%), P = 0.266 • Steatorrhea: 9 (64.3%) vs. 3 (15%), P = 0.003 • Stool elastase (μg/g): 12.7 vs. 50.4, P = NA • Stool elastase No Two-layer, interrupted
PJ PJ, modified side-to-side, duct-to-mucosa PG
One-layer, continuous
Two-layer, interrupted
Two-layered, continuous
Two-layer, interrupted
Two-layer, interrupted
NA
NA
NA
NA
89 ± 49
300
74 (35–410)
394 (80–1500)
295 ± 52
360
357 (270–650)
421 (240–660)
368 (258–608)
456 ± 109.5
300 ± 225
240 (30–1200)
568 (536–629)
476
491.5 ± 94
487.3 ± 121.9
597 (420–960)
392 (327–570)
350 (150–625)
485
247 (50–889)
Transfusion, 31 (31%)
220 (150–400)
NA
541 ± 88
473.75 ± 88.27
Operative time (min)
NA
PPH
1 (9.1)
DGE
0 2
4
2 1
1
NA NA
NA
4 (9.5) 3 (7.3%) 5 (9.5) > grade A > grade A
1 (9.1)
POPF (n, %)
0 2
0
0
BF
16 ± 28
NA
8.2 (6–42)
22 (5–85)
7 (4–69)
8 ± 8.5
10 (8–13)
9.79
13.7 ± 6.1
15 ± 9.7
2
2 (10)
5 (5)
1
NA
5
4
15
11 (18)
1
Yes
NA
2
0, > grade A 2
6 (12), 4 (8) >grade A
2
7 (35)
6 (6)
1
NA
NA
NA
9 (15)
3
5
1
1 (5)
2 (2)
NA
NA
2
NA
NA
NA
NA
0
NA
WI
0
NA
NA
NA NA
NA
NA
Yes
1
NA
NA
MS
8
NA
NA
NA
NA
NA
4 (6)
1
4 (8)
2
1 (5)
2 (2)
NA
NA NA
NA
1
0
1 (1.3)
3 (5)
1 (1.6)
1 (7)
1 (2)
1
0
1
0
1
3
NA
3
4 (2.9)
3
1
3
3
2
1
3
2
0
Mortality Reoperation
10 (18.9) 6 (11.3) 3 (5.7)
0
IAA
3 (15) 2 (10)
3 (3)
0 1 0 23 (10–86) 4 > grade A 2 grade > A 1 > grade A 0
8 ± 3.2
18.14 ± 5.99
LOH (day)
BF biliary fistula, DGE delayed gastric emptying, IAA intraabdominal abscess, LOH length of hospital stay, POPF postoperative pancreatic fistula, PPH postpancreatectomy hemorrhage, WI wound infection.
Palanivelu et al. [51] Gumbs et al. [52] Dulucq et al. [53]
Blood loss (ml)
One-layer, 1106 ± 52.67 interrupted, binding ligature Two-layer, 195 ± 136 interrupted
Suture type
NA
Yes
NA
Yes (43)
Yes
Yes
NA
NA
NA
39
1/10
Stent (no/yes)
PG
PJ duct-to-mucosa
PJ duct-to-mucosa
2012 50 (N/A)
Giulianotti 2010 60 (10.4) et al. [50]
Nguyen et al. [47] Zureikat et al. [67] Kendrick et al. [49]
Pancreatic duct occlusion (cyanoacrylate) PG PJ end-to-side, invagination PJ duct-to-mucosa PJ end-to-side, invagination /PJ duct-to-mucosa PJ end-to-side, invagination, small p-duct/PJ duct-to-mucosa, large p-duct PJ end-to-side, invagination, small p-duct (≤3 mm)/PJ duct-to-mucosa, large p-duct (>3 mm) PJ duct-to-mucosa
PJ duct-to-mucosa
PJ sleeve reconstruction, end-to-end
Technique
R* lap resection+ robot reconstruction R
R
L
2013 90 (4.8)
2012 20 (5)
R
L
L
3 (9.1) 2013 34 (0)
3 10
Chalikonda 2012 30 (10) et al. [46]
Lai et al. [45]
Boggi et al. [43] Kim et al. [44]
2012 41 (16.9)
Asbun et al. [38]
6
2013 11 (NA)
Lei et al. [41]
L
Year Patients Surgical number approach (conversion rate, %)
Authors
Table 5 Summary of the literature reporting laparoscopic pancreaticoduodenectomy
Intestinal obstruction (1), gastroduodenal stenosis (1), tube-gastrostomy
POPF (1), biliary fistula (1), A-loop obstruction (1)
Peritonitis after PG (1), wound debridement (1), esophageal rupture (1), massive colonic ischemia (1)
POPF (1), bleeding (1), biliary fistula (1)
Gastric staple line bleeding (1)
POPF (2), intestinal obstruction (1)
POPF (2), wound dehiscence (1)
Bleeding from POPF (1), ischemic colon (1)
Bleeding (1)
Bleeding (3)
Bleeding and jejunal stump leakage (1), afferent loop obstruction (1)
J Hepatobiliary Pancreat Sci (2015) 22:202–210 207
208
by a backhanded stitch technique with the Haenawa. Ductto-mucosa anastomosis or an internal drainage technique was used for inner layer anastomosis, and in the case of a soft pancreas with a small pancreatic duct, a short stent tube was inserted into the small jejunal orifice after fixation to the main pancreatic duct. After managing the inner layer, serial approximations of Haenawa sutures can be used to complete PJ. It was reported that among 17 patients who underwent laparoscopic PJ with the Haenawa technique, two patients developed clinically relevant POPF, which was managed with conservative measures. Nakamura et al. [11] described another reliable PJ method with closure of the pancreatic stump by an endoscopic linear stapler in lap-PD. This reconstruction technique is a manual reconstruction through a small external wound. The remaining staples ligating the main pancreatic duct were removed to open the main pancreatic duct, and the stent tube was inserted for manual duct-to-mucosa PJ. Additional staples in the pancreatic parenchyma outside the main pancreatic duct were left in place in order to prevent leakage of pancreatic juice from the branches of the pancreatic duct. This technique is modified from a previous report from the Fundan University group in China [60]. Instead of manual closure of the remnant pancreatic stump in an interrupted fashion by inverting sutures with a stent tube in the main pancreatic duct, Nakamura et al. used a stapler in the laparoscopic environment. It was reported that only one patient (5.9%) experienced POPF among 17 patients with this PJ technique following lap-PD.
Discussion In 1994, Gagner and Pomp [61] reported the first successful lap-PD in a 30-year-old female patient with chronic pancreatitis and demonstrated the technical feasibility of a laparoscopic approach to pancreatic head lesions; however, it was thought that the potential benefit of such a minimally invasive surgery may not be as apparent as that of a more common less complex surgical procedure because of technical complexity and potential postoperative high morbidity. Several other clinical series reporting surgical experiences of lap-PD reached similar conclusions [62–64]. Since then, lap-PD was regarded as a myth in the laparoscopic surgical field. However, in 2007, ground-breaking literature was published by Palanivelu et al. [65] from India, inspiring renewed interest in lap-PD. They reported 42 patients who underwent lap-PD, and more surprisingly, most patients (40 out of 42 patients) had periampullary cancers. They described the surgical techniques, comparable perioperative results, and acceptable long-term oncologic outcomes, suggesting that lap-PD can be performed safely and with good
J Hepatobiliary Pancreat Sci (2015) 22:202–210
surgical results in well-selected patients. After their reports and video presentation were released, many laparoscopic surgeons attempted to perform lap-PD relying on their own accumulated laparoscopic experience, techniques and advanced instruments. As a result, several promising reports have recently been reproduced in highly specialized medical centers [44, 49, 51], and some expert surgeons agree that lap-PD is safe and its perioperative outcomes are comparable to those of an open approach [38, 66]. In general, the following questions are relevant when choosing a surgical technique in daily clinical practice: (1) Is it simple? (2) Is it technically easy and feasible? (3) Is it secure and safe? (4) Is there any supporting scientific evidence? According to a literature review of the current practice of laparoscopic reconstruction techniques for the remnant pancreas following PD, in spite of technical variations, PJ (ductto-mucosa or end-to-side PJ) was found to be the most popular procedure following lap-PD. In an open surgical environment, the clinical evidence suggests that there are no superior surgical options for reconstruction of the remnant pancreas following PD. It may depend on the surgeons’ expertise, experience, the texture of the pancreas, and the patient’s condition. These accumulating data can be used as indirect evidence in choosing a laparoscopic pancreatic reconstruction technique; however, laparoscopic PG may not be appropriate, because of the specific anatomic relationship between the stomach and the remnant pancreas, which makes PG more difficult in laparoscopic circumstances. Laparoscopic PJ (duct-to-mucosa) is technically feasible, but it might be somewhat complicated, and technically very difficult in the case of a soft pancreas with a small pancreatic duct. To the contrary, laparoscopic end-to-side PJ (dunking) method is thought to be another good option in managing the remnant pancreas following lap-PD. It is a relatively simple technique and can be performed even in a soft pancreas with a small pancreatic duct. This surgical technique is strongly supported by a previous randomized controlled study and abundant experiences [58]. However, “appropriate surgical technique” may depend on patients’ conditions, surgeons’ experience/technique, and hospital facility with available perioperative management. Ideally, multicenter randomized controlled trial with strict standardized surgical techniques is required to provide a proper answer to this question, but technically it might be very difficult. Acknowledgments Some part of this manuscript was presented in the Symposium: How to Manage the Remnant Pancreas After Laparoscopic Pancreaticoduodenectomy (8TH International Single Topic Symposium of the Korean Association of HBP surgery, on 13 October 2013, Cheongju, South Korea). The authors would like to express sincere gratitude to their international colleagues; Dr Yoshiharu Nakamura (Nippon Medical School), Dr Akira Matsushita (Nippon
J Hepatobiliary Pancreat Sci (2015) 22:202–210 Medical School), and Yuichi Nagakawa (Tokyo Medical University) for providing their valuable comments, which improved the content of this paper. Conflict of interest
None declared.
References 1. Gagner M, Pomp A, Herrera MF. Early experience with laparoscopic resections of islet cell tumors. Surgery. 1996;120: 1051–4. 2. Jin T, Altaf K, Xiong JJ, Huang W, Javed MA, Mai G, et al. A systematic review and meta-analysis of studies comparing laparoscopic and open distal pancreatectomy. HPB. 2012;14:711–24. 3. Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg. 2012;255:1048–59. 4. Pericleous S, Middleton N, McKay SC, Bowers KA, Hutchins RR. Systematic review and meta-analysis of case-matched studies comparing open and laparoscopic distal pancreatectomy: is it a safe procedure? Pancreas. 2012;41:993–1000. 5. Ramacciato G, Mercantini P, Petrucciani N, Nigri GR, Kazemi A, Muroni M, et al. Risk factors of pancreatic fistula after pancreaticoduodenectomy: a collective review. Am Surg. 2011;77:257– 69. 6. Ball CG, Howard TJ. Does the type of pancreaticojejunostomy after Whipple alter the leak rate? Adv Surg. 2010;44:131–48. 7. 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;10:1199–210. 8. Pratt WB, Maithel SK, Vanounou T, Huang ZS, Callery MP, Vollmer CM, Jr. Clinical and economic validation of the International Study Group of Pancreatic Fistula (ISGPF) classification scheme. Ann Surg. 2007;245:443–51. 9. Buchler MW, Friess H, Wagner M, Kulli C, Wagener V, Z’Graggen K. Pancreatic fistula after pancreatic head resection. Br J Surg. 2000;87:883–9. 10. Lee JS, Han JH, Na GH, Choi HJ, Hong TH, You YK, et al. Laparoscopic pancreaticoduodenectomy assisted by minilaparotomy. Surg Laparosc Endosc Percutan Tech. 2013;23:e98– 102. 11. Nakamura Y, Matsumoto S, Matsushita A, Yoshioka M, Shimizu T, Yamahatsu K, et al. Pancreaticojejunostomy with closure of the pancreatic stump by endoscopic linear stapler in laparoscopic pancreaticoduodenectomy: a reliable technique and benefits for pancreatic resection. Asian J Endosc Surg. 2012;5:191–4. 12. Narula VK, Mikami DJ, Melvin WS. Robotic and laparoscopic pancreaticoduodenectomy: a hybrid approach. Pancreas. 2010;39: 160–4. 13. Kim SW, Youk EG, Park YH. Comparison of pancreatogastrostomy and pancreatojejunostomy after pancreatoduodenectomy performed by one surgeon. World J Surg. 1997;21: 640–3. 14. Takano S, Ito Y, Watanabe Y, Yokoyama T, Kubota N, Iwai S. Pancreaticojejunostomy versus pancreaticogastrostomy in reconstruction following pancreaticoduodenectomy. Br J Surg. 2000;87:423–7. 15. Fujino Y, Suzuki Y, Ajiki T, Tanioka Y, Ku Y, Kuroda Y. Risk factors influencing pancreatic leakage and the mortality after pancreaticoduodenectomy in a medium-volume hospital. Hepatogastroenterology. 2002;49:1124–9.
209
16. Schlitt HJ, Schmidt U, Simunec D, Jager M, Aselmann H, Neipp M, et al. Morbidity and mortality associated with pancreatogastrostomy and pancreatojejunostomy following partial pancreatoduodenectomy. Br J Surg. 2002;89:1245–51. 17. Oussoultzoglou E, Bachellier P, Bigourdan JM, Weber JC, Nakano H, Jaeck D. Pancreaticogastrostomy decreased relaparotomy caused by pancreatic fistula after pancreaticoduodenectomy compared with pancreaticojejunostomy. Arch Surg. 2004;139:327–35. 18. Yang SH, Dou KF, Sharma N, Song WJ. The methods of reconstruction of pancreatic digestive continuity after pancreaticoduodenectomy: a meta-analysis of randomized controlled trials. World J Surg. 2011;35:2290–7. 19. Wente MN, Shrikhande SV, Muller MW, Diener MK, Seiler CM, Friess H, et al. Pancreaticojejunostomy versus pancreaticogastrostomy: systematic review and meta-analysis. Am J Surg. 2007;193:171–83. 20. Yeo CJ, Cameron JL, Maher MM, Sauter PK, Zahurak ML, Talamini MA, et al. A prospective randomized trial of pancreaticogastrostomy versus pancreaticojejunostomy after pancreaticoduodenectomy. Ann Surg. 1995;222:580–8; discussion 8–92. 21. Duffas JP, Suc B, Msika S, Fourtanier G, Muscari F, Hay JM, et al. A controlled randomized multicenter trial of pancreatogastrostomy or pancreatojejunostomy after pancreatoduodenectomy. Am J Surg. 2005;189:720–9. 22. Fernandez-Cruz L, Cosa R, Blanco L, Lopez-Boado MA, Astudillo E. Pancreatogastrostomy with gastric partition after pylorus-preserving pancreatoduodenectomy versus conventional pancreatojejunostomy: a prospective randomized study. Ann Surg. 2008;248:930–8. 23. Topal B, Fieuws S, Aerts R, Weerts J, Feryn T, Roeyen G, et al. Pancreaticojejunostomy versus pancreaticogastrostomy reconstruction after pancreaticoduodenectomy for pancreatic or periampullary tumours: a multicentre randomised trial. Lancet Oncol. 2013;14:655–62. 24. Figueras J, Sabater L, Planellas P, Muñoz-Forner E, Lopez-Ben S, Falgueras L, et al. Randomized clinical trial of pancreaticogastrostomy versus pancreaticojejunostomy on the rate and severity of pancreatic fistula after pancreaticoduodenectomy. Br J Surg. 2013;100:1597–605. 25. Menahem B, Guittet L, Mulliri A, Alves A, Lubrano J. Pancreaticogastrostomy is superior to pancreaticojejunostomy for prevention of pancreatic fistula after pancreaticoduodenectomy: an updated meta-analysis of randomized controlled trials. Ann Surg. 2014; doi: 10.1097/SLA.0000000000000806. 26. Liu FB, Chen JM, Geng W, Xie SX, Zhao YJ, Yu LQ, et al. Pancreaticogastrostomy is associated with significantly less pancreatic fistula than pancreaticojejunostomy reconstruction after pancreaticoduodenectomy: a meta-analysis of seven randomized controlled trials. HPB (Oxford). 2014; doi: 10.1111/hpb.12279. 27. Reid-Lombardo KM, Ramos-De la Medina A, Thomsen K, Harmsen WS, Farnell MB. Long-term anastomotic complications after pancreaticoduodenectomy for benign diseases. J Gastrointest Surg. 2007;11:1704–11. 28. Morera-Ocon FJ, Sabater-Orti L, Munoz-Forner E, Perez-Griera J, Ortega-Serrano J. Considerations on pancreatic exocrine function after pancreaticoduodenectomy. World J Gastrointest Oncol. 2014;6:325–9. 29. Kim JH, Yoo BM, Kim JH, Kim WH. Which method should we select for pancreatic anastomosis after pancreaticoduodenectomy? World J Surg. 2009;33:326–32. 30. Tomimaru Y, Takeda Y, Kobayashi S, Marubashi S, Lee CM, Tanemura M, et al. Comparison of postoperative morphological changes in remnant pancreas between pancreaticojejunostomy and pancreaticogastrostomy after pancreaticoduodenectomy. Pancreas. 2009;38:203–7.
210 31. Fang WL, Su CH, Shyr YM, Chen TH, Lee RC, Tai LC, et al. Functional and morphological changes in pancreatic remnant after pancreaticoduodenectomy. Pancreas. 2007;35:361–5. 32. Jang JY, Kim SW, Park SJ, Park YH. Comparison of the functional outcome after pylorus-preserving pancreatoduodenectomy: pancreatogastrostomy and pancreatojejunostomy. World J Surg. 2002;26:366–71. 33. Chou FF, Sheen-Chen SM, Chen YS, Chen MC, Chen CL. Postoperative morbidity and mortality of pancreaticoduodenectomy for periampullary cancer. Eur J Surg. 1996;162:477–81. 34. 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– 71. 35. Langrehr JM, Bahra M, Jacob D, Glanemann M, Neuhaus P. Prospective randomized comparison between a new mattress technique and Cattell (duct-to-mucosa) pancreaticojejunostomy for pancreatic resection. World J Surg. 2005;29:1111–19; discussion 20-1. 36. 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;208:738–47. 37. 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;245:692–8. 38. Asbun HJ, Stauffer JA. Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J Am Coll Surg. 2012;215:810–19. 39. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, et al. Comparison of laparoscopy-assisted and open pylorus-preserving pancreaticoduodenectomy for periampullary disease. Am J Surg. 2009;198:445–9. 40. Choi SH, Kang CM, Kim DH, Lee WJ, Chi HS. Robotic pylorus preserving pancreaticoduodenectomy with mini-laparotomy reconstruction in patient with ampullary adenoma. J Korean Surg Soc. 2011;81:355–9. 41. Lei Z, Zhifei W, Jun X, Chang L, Lishan X, Yinghui G, et al. Pancreaticojejunostomy sleeve reconstruction after pancreaticoduodenectomy in laparoscopic and open surgery. JSLS. 2013; 17:68–73. 42. Corcione F, Pirozzi F, Cuccurullo D, Piccolboni D, Caracino V, Galante F, et al. Laparoscopic pancreaticoduodenectomy: experience of 22 cases. Surg Endosc. 2013;27:2131–6. 43. Boggi U, Signori S, De Lio N, Perrone VG, Vistoli F, Belluomini M, et al. Feasibility of robotic pancreaticoduodenectomy. Br J Surg. 2013;100:917–25. 44. Kim SC, Song KB, Jung YS, Kim YH, Park do H, Lee SS, et al. Short-term clinical outcomes for 100 consecutive cases of laparoscopic pylorus-preserving pancreatoduodenectomy: improvement with surgical experience. Surg Endosc. 2013;27:95–103. 45. Lai EC, Yang GP, Tang CN. Robot-assisted laparoscopic pancreaticoduodenectomy versus open pancreaticoduodenectomy —a comparative study. Int J Surg. 2012;10:475–9. 46. Chalikonda S, Aguilar-Saavedra JR, Walsh RM. Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg Endosc. 2012;26:2397–402. 47. Nguyen KT, Zureikat AH, Chalikonda S, Bartlett DL, Moser AJ, Zeh HJ. Technical aspects of robotic-assisted pancreaticoduodenectomy (RAPD). J Gastrointest Surg. 2011;15:870–5.
J Hepatobiliary Pancreat Sci (2015) 22:202–210 48. Abood GJ, Can MF, Daouadi M, Huss HT, Steve JY, Ramalingam L, et al. Robotic-assisted minimally invasive central pancreatectomy: technique and outcomes. J Gastrointest Surg. 2013;17: 1002–8. 49. Kendrick ML, Cusati D. Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg. 2010;145:19–23. 50. Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P, et al. Robot-assisted laparoscopic pancreatic surgery: singlesurgeon experience. Surg Endosc. 2010;24:1646–57. 51. Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, et al. Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg. 2009; 16:731–40. 52. Gumbs AA, Gres P, Madureira FA, Gayet B. Laparoscopic vs. open resection of noninvasive intraductal pancreatic mucinous neoplasms. J Gastrointest Surg. 2008;12:707–12. 53. Dulucq JL, Wintringer P, Mahajna A. Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surg Endosc. 2006;20:1045–50. 54. Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, et al. Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg. 2000;4:567–79. 55. Schnelldorfer T, Ware AL, Sarr MG, Smyrk TC, Zhang L, Qin R, et al. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma: is cure possible? Ann Surg. 2008;247: 456–62. 56. Kang CM, Kim DH, Lee WJ, Chi HS. Initial experiences using robot-assisted central pancreatectomy with pancreaticogastrostomy: a potential way to advanced laparoscopic pancreatectomy. Surg Endosc. 2011;25:1101–6. 57. Giulianotti PC, Sbrana F, Bianco FM, Addeo P, Caravaglios G. Robot-assisted laparoscopic middle pancreatectomy. J Laparoendosc Adv Surg Tech A. 2010;20:135–9. 58. Eugene P, Kennedy CJY. Dunking pancreaticojejunostomy versus duct-to-mucosa anastomosis. J Hepatobiliary Pancreat Sci. 2011; 18:769–74. 59. Honda G, Kurata M, Okuda Y, Kobayashi S, Yamaguchi T, Matsumoto H, et al. Novel device for pancreaticojejunostomy via a pure laparoscopic approach. J Am Coll Surg. 2013;216:e73–6. 60. Liu C, Long J, Liu L, Xu J, Zhang B, Yu X, et al. Pancreatic stump-closed pancreaticojejunostomy can be performed safely in normal soft pancreas cases. J Surg Res. 2012;172:e11–7. 61. Gagner M, Pomp A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc. 1994;8:408–10. 62. Cuschieri A. Laparoscopic pancreatic resections. Semin Laparosc Surg. 1996;3:15–20. 63. Park A, Schwartz R, Tandan V, Anvari M. Laparoscopic pancreatic surgery. Am J Surg. 1999;177:158–63. 64. Underwood RA, Soper NJ. Current status of laparoscopic surgery of the pancreas. J Hepatobiliary Pancreat Surg. 1999;6:154–64. 65. Palanivelu C, Jani K, Senthilnathan P, Parthasarathi R, Rajapandian S, Madhankumar MV. Laparoscopic pancreaticoduodenectomy: technique and outcomes. J Am Coll Surg. 2007; 205:222–30. 66. Cho A, Yamamoto H, Nagata M, Takiguchi N, Shimada H, Kainuma O, et al. Laparoscopic major hepato-biliary-pancreatic surgery: formidable challenge to standardization. J Hepatobiliary Pancreat Surg. 2009;16:705–10. 67. Zureikat AH, Breaux JA, Steel JL, Hughes SJ. Can laparoscopic pancreaticoduodenectomy be safely implemented? J Gastrointest Surg. 2011;15:1151–7.
