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Laparoscopic pancreatic surgery 329
Fernandez-Cruz et al. reporteda 35% incidence of POPF in
Lap EN compared with both spleen-preserving LDP
(7.7%) and LDP with splenectomy (10%) [45]. Other
series report morbidity and POPF of 17–42% and
13–35%, respectively, but these studies are hindered by
various definitions of POPF and use of the Clavien–Dindo
classification of morbidity [44,45,48,53]. Furthermore,
drain placement, use of somatostatin analogues, and postoperative imaging varies as well, indicating that morbidity
and fistula rates may be underreported in these studies.
With regard to oncological parameters and long-term
outcomes, Lap EN data are sparse. Crippa et al. suggested
lymph node sampling during Lap EN procedures with
conversion to pancreatectomy if nodal involvement is confirmed at the time of surgery [51]. Other authors have
endorsed traditional resection over Lap EN for any neuroendocrine pathology other than insulinoma [54]. In the
Costi series, nine patients had malignant pathology at the
time of operation and the authors followed patients for an
average of 81 months. There was no local recurrence in any
of the patients with malignant pathology, but the authors
found three patients (33%) with regional recurrence of
malignancy in the follow-up period [49]. Lap EN appears
safe and feasible for well-selected benign tumors, but the
literature supports more formal surgical approaches for
larger benign disease and frank malignancy.
23.4 Laparoscopic
pancreaticoduodenectomy
Laparoscopic pancreaticoduodenectomy (LPD) was first
described in 1994 by Gagner and Pomp in an advanced
laparoscopic surgical trial to reduce postoperative morbidity [55]. This was followed by a series of 10 patients
three years later that demonstrated a high conversion rate
(40%) and long operating time (510 min) [56]. The
complicated procedure demands careful dissection near
the portal vein confluence during resection and then
creation of three reconstructive anastomoses (biliary,
intestinal, pancreatic) requiring laparoscopic suturing.
In the nearly 20 years since it was introduced, a handful
of case reports and retrospective series from high-volume
institutions have been published on LPD, showing it to be
both safe and feasible [56–61]. Some surgeons have
reported favorable operative outcomes of LPD over
OPD, but selection and reporting bias are possible confounding factors to be considered [57,62,63]. In the
literature, oncological parameters, including margin status and nodal retrieval, are similar between LPD and OPD
in comparison series, but again selection bias appears
towards small, right-sided malignancies in the laparoscopic cohorts [64].
Given the technical challenges of LPD, stringent patient
selection guidelines have been followed by surgeons
conducting the operation. Nonobese patients are more
amenable to laparoscopic resection as the presence of
excessive adiposity in the omentum makes the procedure
more difficult. The following selection parameters are
typically adhered to for eligible patients:
• pancreatic head tumors <3 cm in diameter without
evidence of vascular invasion
• well-differentiated or moderate-grade ampullary
tumors restricted to the second part of the duodenum
• lower common bile duct tumors without extrabiliary
involvement [57].
Preoperative imaging using helical computed tomography (CT) or endoscopic ultrasound (US) is a useful
adjunct to carefully defining tumor extension. The technical details of LPD have been given previously in the
literature [55,57,58]. While no standard procedure exists,
some centers favor a hand-assist approach for
reconstruction while others undertake the procedure
completely laparoscopically (Figure 23.5) [57,65].
Conversions to the open approach are typically for
tumor adhesion to the portal vein, uncontrolled bleeding,
and failure to progress[58,64]. While earlierseries showed
a preference for resection of benign disease, recent publications demonstrate that more malignant cases are
selected, however carefully, for laparoscopic resection.
With regard to malignancy, some authors prefer resecting
ampullary adenocarcinoma laparoscopically because of its
further distance from the SMA and SMV while other
centers have selected pancreatic adenocarcinoma for
resection with adequate margin status [4,29,57,59].
While the last four years have seen a rise in the number
of published analyses of LPD, to date only seven papers
feature 25 or more patients [57–59,64,66–68]. Average
mean operating time is 440 minutes. Kim et al. noted a
stepwise decrease in their median operative time with
greater surgeon experience. Compared with their first
30 cases, where median operative time was 588 minutes,
subsequent breakdown of an additional 70 cases showed
OR time decreased to 474 and then 396 minutes [67].
Along with decreased operative times, published conversion rates in high-volume series have seen a decline,
330 Chapter 23
from 40% reported by Gagner et al. down to an average of
6.8% in the last three years [29,63,64,67,68]. Several
centers are reporting 0% conversions [59,66,68]. Similar
trends are evident in estimated blood loss, mean length of
hospital stay, and morbidity, all likely attributable to greater
surgeon proficiency and refined technique (Figure 23.6).
Complication rate for LDP varies from 0 to as high as 60%.
Incidence of pancreatic fistula, regardless of definition used,
also has a wide range of 0–36% [59,64,66,67,69]. Mortality
is low in LPD, with most series reporting 0–3 total deaths in
the perioperative period (Table 23.2).
A few studies have directly compared LPD with the
open procedure [4,60,64,69]. Chalikonda et al. noted
similar morbidity (30% vs 44%, P = 0.14) in an analysis
of 30 cases of minimally invasive LPD compared with
open PD [69]. The minimally invasive cohort had
decreased length of stay (9.79 days vs 13.26 days,
P = 0.043) and a longer operating time (476.2 min vs
366.4 min P = 0.0005) as well [69]. Pugliese et al. found
no significant differences in morbidity (45% in LPD vs
Figure 23.5 Typical port positions for LPD. Source: Kim et
al. [67]. Reproduced with permission of Springer.
44% in OPD), incidence of POPF (27% for both LPD and
OPD) or hospital length of stay (18 days in LPD vs 18 days
in OPD) in a comparison of 13 LPD with 41 open
cases [60]. Cho retrospectively compared 15 LPD and
15 OPD and found no statistically significant differences in
morbidity (27% vs 26%), blood loss (445 ± 384 mL vs
552 ± 336 mL), or hospital stay (16.4 ± 3.7 days vs
15.6 ± 1.3 days) [4]. Kendrick reported decreased blood
loss (400 vs 600 mL, P < 0.001) and hospital length of stay
(6 vs 10 days, P < 0.001) in his center’s comparison series
of 52 LPD and 129 OPD [68]. Asbun et al. compared 53
LPD vs 215 OPD over a six-year period at the Mayo Clinic
Florida which demonstrated a significant decrease in EBL
(195 vs 1032 mL, P < 0.001), transfusion requirement
(0.6 vs 4.7 units, P < 0.001), intensive care unit (ICU)
stay (1 vs 3 days, P < 0.001) and hospital length of stay
(8 vs 12.4 days, P < 0.001) in the LPD cohort [64]. Morbidity rates were equal (24.5% vs 24.7%) as well as the
proportion of clinically significant (grade B/C) fistula
(11% vs 15.3%) [64]. These are all unmatched,
Laparoscopic pancreatic surgery 331
Figure 23.6 Decreased OR time, hospital stay, and morbidity with increased surgeon experience [67].
retrospective studies with relatively small sample sizes but
they demonstrate a trend toward beneficial perioperative
outcomes for LPD in well-selected patients.
With regard to oncological considerations, there is a
greater proportion of malignant cases in the LPD literature
than in other laparoscopic pancreatic publications. Of the
papers reporting tumor size, the average is 2.6 cm which
corresponds to the trend of selecting small, circumscribed
lesions for laparoscopic resection [57–59,64]. Mean nodal
retrieval is 17, with ranges of 3–34 procured, and authors
have achieved R0 margins in over 97% of LPD resections
of malignancy. Kendrick reported equivocal outcomes for
tumor size (3.2 vs 3.4 cm), margin-negative resection
(83% vs 83%), and number of lymph nodes harvested
(17 vs 18) in a recent analysis of 52 laparoscopic resections
of PDAC compared with 129 open resections of the same
pathology [68]. In their comparison of LPD vs OPD at the
Mayo Clinic Florida, Asbun et al. reported superior nodal
retrieval in the LPD cohort (23.44 vs 16.84 nodes,
P < 0.001). This translated to lower lymph node ratio for
those patients with node-positive disease undergoing the
laparoscopic approach (0.159 vs 0.241, P = 0.0072). Furthermore, they achieved R0 margins in 94.9% of laparoscopic cases versus only 83% in the open cohort, although
this difference was not statistically significant [64].
Substantial long-term oncological outcomes for LPD
are not readily available owing to the paucity of literature
published to date. Median follow-up is 17 months and, for
papers reporting recurrences rates, these average 17.5%
(range 7.5–38%) [57,58,60,67]. In their first series, Palanivelu et al. showed median survival of 49 months with a
five-year actuarial survival rate of 32% among the 40
patients with malignancy [57]. However, there was selection bias for early malignant lesions to be resected laparoscopically. Additional data on long-term survival will
likely come with further patient surveillance.
This review demonstrates that LPD is a safe, feasible,
and noninferior approach to resection of right-sided pancreatic lesions, both benign and malignant, in wellselected patients at high-volume centers. Randomized
332 Chapter 23
Table 23.2 Summary of laparoscopic pancreaticoduodenectomy in the literature
Author (year) No. of Benign Malignant Pathology Conversion Hand Mean Mean Mean Postoperative Pancreatic Mortality Tumor Mean Positive Median Recurrence
Gagner et al. 10 2 8 4 PDAC, 3 AMP, 40 33 510 NR 22.3 50 17 0 NR 7 (3–14) 0 19 NR
(1997) [56] 2 pancreatitis,
Staudacher et al. 7 2 2 2 PNET, 1 PDAC, 1 MM, 43 100 416 325 12 0 0 0 NR 26 0 4.5 NR
(2005) [65] 3 not recorded (16–47)
Lu et al. (2006) [61] 5 0 5 4 duodenal adenocarcinoma, 0 0 528 770 NR 60 20 20 NR NR NR NR NR
Dulucq et al. 25 3 19 11 PDAC, 4 AMP, 2 DA, 12 41 287 107 16.2 32 4.5 4.5 2 18 (---) 0 19.2 11
(2006) [58] 1 PNET, 2 CP, 1 RCC, 1SCA
Palanivelu et al. 42 2 40
(2007) [57] 3 CC 2 pancreatitis (18–21)
Pugliese et al. 19 1 18 11 PDAC, 4 AMP, 3 CC, 32 54 461 180 18 37 23 0 2.5 12 (4–22) 0 32 33
(2008) [60] 1 mesenchymal tumor
Cho et al. (2009) [4] 15 7 8
Palanivelu et al. 75 3 72 29 AMP, 23 PDAC, 10MCA, 0 0 357 74 8.2 26 7 1.33 NR 14 (8–22) 2.6 NR NR
(2009) [66] 10 CC, 3 CP
Asbun et al. 53 14 39
(2012) [64]
Kendrick and Cusati 65 19 46
(2010) [59]
patients Rate (%) assist operative blood Length Morbidity Fistula (%) Size nodes Margins Follow- (%)
1 cholangiocarcinoma
1 PNET
24 AMP, 9 PDAC, 4 MCA, 0 0 370 65 10.2 NR 7.1 2.4 2.9 13 0 36.5 7.5
6 mucinous adenoma, 0 100 338 445 16.4 27 13 0 NR 18.5 (---) 0 NR NR
3 MCA, 2 PNET,
1 AMP, 1 PDAC,
1 duodenal
plasmacytoma,
1 pancreatic trauma
22 PDAC, 8 IPMN, 6 15 5.6 541 195 8 45.3 16.7 5.7 2.7 23 (---) 5.1 3.33 NR
PNET, 8 AMP, 2 SCA,
3 CC, 1 solid
pseudopapillary
neoplasm,
1 GIST, 2 CP
32 PDAC, 12 IPMN, 4.6 0 368
8 AMP, 4 NET, 3 CP,
1 CC,1 RCC,
1 cystadenoma,
1 duodenal
adenoma
(%) time loss of Stay rate (%) rate (%) (cm)
(min) (mL) (days) (range) (months)
∗
240∗7
∗
42 18 1.6 3 15 11 7.2 16
∗∗∗∗
procured (%)
∗
(6–31)
∗∗∗∗
up
∗∗∗∗
Laparoscopic pancreatic surgery 333
Suzuki et al. 6 1 5 4 AMP, 1 PDAC, 1 IPMN 0 100 581∗471∗23∗33.3 33.3 0 NR 18 036 NR
(2011) [70] (16–27)
Ammori and 7 0 7 5 PDAC, 2 AMP 0
Ayiomamitis (11–32)
(2011) [29]
Zureikat et al. 14 2 12 8 PDAC, 2 CC, 1 duodenal 14 0 456
(2011) [71] adenocarcinoma, 1 GIST,
Kendrick (2012) [68] 52 0 52 52 PDAC 0 0 370 400 6 NR NR NR 3.2 17 17 24 38
Kim et al. (2013) [67] 100 88 12
Totals 495 142 343
Means 10.1 24.5 12.4 29.9 440.0 291.1 13.0 36.0 16.4 3.1 2.7 17 2.7 17.2 17.6
AMP, ampullary adenocarcinoma; CC, cholangiocarcinoma; CP, chronic pancreatitis; DA, duodenal adenocarcinoma; GIST, gastrointestinal stromal tumor; IPMN, intraductal papillary mucinous neoplasm; MCA,
mucinous cystadenoma; MM, malignant melanoma; NET, neuroendocrine tumor; PDAC, pancreatic ductal adenocarcinoma; PNET, pancreatic neuroendocrine tumor; RCC, renal cell carcinoma; SCA, serous
cystadenoma.
1 IPMN, 1 CP
37 IPMN, 17 solid 4.7
pseudopapillary
tumors, 15 PNET,
7 SCA, 7 PDAC,
2 MCA, 5 AMP,
5 duodenal GIST, 1 CP,
1 RCC, 1 CC, 2 benign
cyst
∗∗∗
14.3 628 350 11.11 28.6 28.6 0 NR 20.8 NR 5 NR
∗
∗∗∗∗∗
0 474 NR 15 25 6 1 2.8 13 (7–34) 0 10.2 9.1
300∗8
∗
62 36 7.1 2.2 18.5 (---) 0 9.5 8.3
∗
∗∗
334 Chapter 23
trials of LPD and open procedures are necessary to
strengthen the assessments that can be made when comparing the two groups. With further experience and more
follow-up data on long-term patient outcomes, LPD can
be better utilized for malignancy.
suited best for patients with contained tumors in the
body and tail of the pancreas, and it appears to provide
similar outcomes to open resection, with fewer complications, lower blood loss, and shorter hospital stays for cases of
similar difficulty. Laparoscopic enucleations are less commonly performed but have a role in the management of
indolent small tumors away from the main pancreatic duct.
23.5 Conclusion
The paucity of cases means that randomized evaluation of
the laparoscopic approach and the open approach is not
Through improved technology and growing experience,
laparoscopic pancreatic resections are being performed
more commonly. Laparoscopic distal pancreatectomy is
feasible. Experience with laparoscopic pancreaticoduode-
nectomy is growing, but more data are necessary to prove
the value of this approach against the open procedure.
KEY POINTS
• Distal pancreatectomy can provide comparable oncological outcomes with fewer complications, lower blood loss, and shorter
hospital stay when compared with open surgery.
• Laparoscopic enucleation has an important role in the management of indolent small tumors not involving or approaching the
main pancreatic duct.
• Outcomes of laparoscopic versus open pancreas surgery are difficult to assess because of differences in technique, perioperative
chemotherapy and chemoradiation, patient selection, surgeon and patient bias, and availability of experienced laparoscopic
surgeons.
• Laparoscopic pancreaticoduodenectomy is still in the developmental phase and practiced by a limited number of surgeons in
selected centers.
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techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary
Pancreat Surg 2009; 16(6):731–740.
67 Kim SC, Song K, Jung YS, et al. Short-term clinical outcomes
for 100 consecutive cases of laparoscopic pylorus-preserving
pancreatoduodenectomy: improvement with surgical experience. Surg Endosc 2013; 27(1):95–103.
68 Kendrick ML. Laparoscopic and robotic resection for pancre-
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69 Chalikonda S, Aguilar-Saavedra JR, Walsh RM. Laparoscopic
robotic-assisted pancreaticoduodenectomy: a case-matched
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(9):2397–2402.
70 Suzuki O, Kondo S, Hirano S, et al. Laparoscopic pancreati-
coduodenectomy combined with minilaparotomy. Surg
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71 Zureikat AH, Nguyen KT, Bartlett DL, Zeh MJ, Moser AJ.
Robotic-assisted major pancreatic resection and reconstruction.
Arch Surg 2011; 146(3):256–261.
Videos 20–26 will be of interest to readers of this chapter.
Visit the companion website at:
www.wiley.com\go\conrad\liver-pancreas-biliary-laparoscopic-surgery
CHAPTER 24
Indications and contraindications
for laparoscopic pancreas surgery
Hanno Niess and Jens Werner
Department of General, Visceral, Transplantation, Vascular and Thoracic Surgery, Hospital of the University of Munich, Munich, Germany
EDITOR COMMENT
It is important to us that we provide a balanced view on the advantages of laparoscopic surgery in this book. This is especially true for
laparoscopic pancreas surgery, an approach that is in its developmental stages. For this chapter we have elicited the opinion of experts to
provide a critical discussion of the advantages and short-comings of laparoscopic pancreas surgery. The lack of randomized and
prospective data regarding the advantages of a mini mally invasive approach over an open one, as well as some of the technical challenges
of laparoscopic pancreaticoduodenectomy, are highlighted. Nonetheless, the promising available retrospective data on laparoscopic
distal pancreatectomy and pancreatic enucleation are discussed. This chapter concludes with an excellent section on the minimally
invasive management of pancreatitis, focusing on indications for intervention, timing, and approaches. This balanced and sometimes
critical view on minimally invasive pancreas surgery by expert pancreatic surgeons reminds the community of the overall goals of surgery,
which is excellence in outcomes.
Keywords: laparoscopic distal pancreatectomy, laparoscopic enucleation, laparoscopic pancreatectomy, laparoscopic pancreaticoduodenectomy, minimally invasive management of pancreatitis
24.1 Introduction
In a number of abdominal operations, minimally invasive
approaches have yielded favorable outcomes regarding
postoperative pain, blood loss, recovery time, and functional convalescence compared with open surgery. Moreover, the use of laparoscopic surgery, particularly in
patients with colon cancer, has shown that the benefits
of laparoscopy can be achieved without compromises on
oncological outcomes [1].
The benefits of laparoscopic approaches are mainly due
to reduced access trauma and minimal mechanical
abdominal wall and organ retraction. The laparoscopic
approach has therefore become the standard approach for
a majority of abdominal surgeries performed today and
an important pillar of fast-track programs for colorectal
surgery. The downsides of a laparoscopic approach
include difficulties in achieving adequate exposure,
Laparoscopic Liver, Pancreas, and Biliary Surgery: Textbook and Illustrated Video Atlas, First Edition.
Edited by Claudius Conrad and Brice Gayet.
© 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd.
resulting in a narrow working space, limited orientation
in a three-dimensional space, fewer degrees of freedom
with instrumentation as well as decreased haptic feedback. In 2014, at our institution, a minimally invasive
approach was selected for surgeries of the colon, rectum,
appendix, gallbladder, esophagus, and spleen in 50%,
50%, 86%, 76%, 17%, and 43% of cases, respectively.
These case distributions might be reflective of the use of
laparoscopy at referral centers with obligations to complex patient care as well as student and resident training.
Gagner and Cuschieri first successfully used minimally
invasive approaches for major pancreatic resections in
1994 [2,3]. However, the rapid development of this technique to become the widely accepted standard approach in
pancreatic surgery has been limited by several factors,
including the pancreas’ retroperitoneal location and fragility
of the gland, the complexity of the surrounding anatomical
structures, the proximity tomajorbloodvesselsandthe
337
338 Chapter 24
proneness of these procedures to postoperative complications. Laparoscopic surgery in patients with pancreatic
diseases was therefore mainly limited to diagnostic or palliative purposes. With the development of novel energy
devices such as ultrasound dissectors and staplers, more
widespread use of laparoscopic techniques for pancreatic
resections occurred. The resulting case series and studies
indicate promising results of the minimal invasive approach
in selected cases.
The development of laparoscopic pancreas resection mirrors the advancements in laparoscopic colon surgery: in
colon surgery, the indications evolved from benign, such as
diverticulosis, towards malignant tumors over time. In
pancreas surgery, lesions included small endocrine tumors
or in some cases cystadenomas located in the distal pancreas, where no reconstruction following resection is
needed. With increasing experience with the technique,
some surgeons have expanded the indications to small
malignant lesions in the pancreas. However, obtaining a
negative resection margin and performing adequate lymph
node dissection are nonetheless pivotal for oncological
outcome and only sparse data exist indicating equivalence
of open and laparoscopic techniques for pancreas surgery.
Therefore, most surgeons still do not use laparoscopy for
pancreatic surgery or limit the laparoscopic approach to
benign and low-grade malignant lesions confinedtothe
pancreas. In our experience, because of the aggressive
biology of pancreatic cancer, few patients present with
malignant lesions that are eligible for a laparoscopic
approach, which makes these indications at our institution
relatively rare. This in turn reduces the case volume available to ascend the steep learning curve that exists for these
difficult laparoscopic procedures.
Despite the observed overall reduction in the operative
morbidity of pancreatic surgery over the last decades,
these operations are still associated with a high rate of
severe complications and perioperative mortality compared with nonpancreatic procedures. Although the
extent of the access trauma (i.e. laparotomy vs laparoscopy) accounts for some of the overall morbidity, in large
pancreatic resections the procedural trauma may far
exceed the access trauma [4] (Figure 24.3). Proper
Figure 24.1 Examples of indications for the laparoscopic approach in distal pancreatectomy. Representative MR/DOTA-TATE PET CT
images of patients operated on laparoscopically at our institution. Indications were: (a,b) neuroendocrine tumor, (c) mucinous cystic
neoplasia.
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