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Chapter 8 / Minimally Invasive Pancreatic Surgery 91
the pancreas out of the retroperitoneum. e latter approach is most com-
monly used when the parenchymal transection is anticipated to occur
within the pancreatic body rather than the tail.
Pancreatic Resection
With the pancreas elevated o of the splenic vessels, the pancreatic
parenchyma is then divided with either a linear stapler with biologic rein-
forcement or the harmonic scalpel. If spleen preservation is planned, the
assistant retracts the pancreas anteriorly and laterally to expose the dis-
section plane between the pancreas and splenic vessels. Most tributary ves-
sels can be divided with the harmonic scalpel. Larger vessels (≥2mm) are
ligated with suture or are clipped and divided. When planning splenectomy,
the splenic vessels are ligated and divided near the pancreatic transection
site prior to a right-to-left dissection with division of the short gastric ves-
sels and splenic peritoneal attachments.
Specimen Retrieval
e specimen is placed in an endobag and removed via the periumbilical
incision that is extended just long enough to accommodate the specimen.
e specimen is inspected on the back table, and a sep arate pancreatic mar-
gin is harvested. We routinely use frozen section histology for evaluation of
the primary lesion and the margin prior to termination of the procedure.
e extraction site is closed with interrupted suture, leaving the cephalad
two sutures untied. e trocar is reintroduced and the carbon dioxide (CO
2
)
pneumoperitoneum reestablished.
Pancreatic Stump Management and Closure
When the transection is not performed with the stapler, our preferred
method of pancreatic stump treatment is with saline-coupled radiofre-
quency energy source (Salient Surgical Technologies, Portsmouth, NH). e
pancreatic resection bed and exposed splenic vessels are then reinspected,
and hemostasis is ensured. Prophylactic operative drains are not routinely
used in the author’s practice. e trocars are removed, and sites are closed
with a 4-0 subcuticular monolament absorbable suture.
Laparoscopic Pancreaticoduodenectomy
Setup, Access, and Initial Exposure
e patient is positioned supine in 15 degrees of reverse Trendelenburg.
Initial access is gained through a left subcostal site using a 12-mm transpar-
ent, cone-tip trocar. A CO
2
pneumoperitoneum to 15mm Hg is established,
and all visible peritoneal and visceral surfaces are inspected. Five additional
12-mm trocars are placed (Fig. 8.2).
e gastrocolic ligament is divided with the harmonic scalpel (Ethicon
Endosurgery, Cincinnati, OH), widely exposing the lesser sac. e gastroepi-
ploic vessels are clipped and divided with the harmonic scalpel. e duode-
nocolic ligament is resected en bloc with the specimen to facilitate regional
lymphadenectomy. A fan retractor is placed under the gastric antrum to
provide exposure of the pancreatic head and neck.
Pancreatic Neck Dissection
e pancreatic neck is approached with the surgeon positioned on the left
side of the patient. e common hepatic artery lymph nodes are removed,
and the common and proper hepatic arteries are identied to verify tumor
clearance. e portal vein is exposed at the cephalad border of the pan-
creatic neck and the superior mesenteric vein at the caudal border. e
Section I / Pancreas92
gastroduodenal artery is dissected, ligated, clipped, and divided. A plane
between the posterior aspect of the pancreatic neck and the portal vein/
superior mesenteric vein is developed. An articulating grasper is passed
posteriorly and an umbilical tape is placed around the pancreatic neck and
secured.
Duodenal Mobilization
e rst portion of the duodenum is cleared, and the right gastric artery
is ligated and divided. e duodenum is divided 2cm distal to the pylorus
using a linear stapler. e transverse colon is reected cephalad, and the
area of the ligament of Treitz is dissected mobilizing the third and fourth
portions of the duodenum o of the aorta and inferior vena cava. e jeju-
num is divided 15cm distal to the ligament of Treitz with the linear sta-
pler, and the jejunal mesentery is then divided with the harmonic scalpel
back to the uncinate process. e hepatic exure of the colon is mobilized
inferiorly, and the ascending and transverse colon are retracted inferiorly
with a fan retractor. e surgeon moves to the patient’s right side, and
the Kocherization of the duodenum is extended cephalad to the hepatic
hilum.
Hepatic Hilar Dissection
A cholecystectomy is performed, leaving the cystic duct intact. e hilum
of the liver is dissected, and the common hepatic duct is identied, ligated
distally, and divided. All hilar lymphatic tissue is dissected inferiorly with
the specimen. e lateral aspect of the portal vein is cleared caudally until
10 mm
10 mm
10 mm
10 mm
10 mm
10 mm
5 cm
FIGURE 8.2 Trocar positioning for laparoscopic
pancreaticoduodenectomy.
Chapter 8 / Minimally Invasive Pancreatic Surgery 93
the superior pancreaticoduodenal vein is identied, ligated, and divided.
e jejunal stump is brought into the supramesocolic compartment, and
the anterolateral aspect of the superior mesenteric vein is dissected proxi-
mally to the inferior border of the pancreas.
Pancreatic Head Resection
e pancreatic neck is divided with the harmonic scalpel, with the excep-
tion of the pancreatic duct, which is divided sharply with scissors. Using
the umbilical tape for retraction, the pancreatic head and uncinate process
are dissected o the portal vein, superior mesenteric vein, and superior
mesenteric artery (SMA). e inferior pancreaticoduodenal artery and vein
are ligated or clipped and divided with harmonic scalpel. Dissection of the
uncinate is performed adjacent to the adventitia of the SMA to assure an
appropriate oncologic margin.
Specimen Removal
e specimen is placed into an endobag and removed via the infraumbili-
cal trocar site, which is typically extended to a total length of 3 to 5cm to
accommodate the specimen. Specimen inspection is performed on the
back table; separate pancreatic neck and bile duct margin are harvested
and sent for frozen section analysis. e portal vein groove and SMA mar-
gins are inked. e extraction site is closed with interrupted suture and a
CO
2
pneumoperitoneum reestablished.
Anastomotic Reconstruction
e jejunum is brought through the duodenal resection bed (retromes-
enteric tunnel). An end-to-side pancreaticojejunostomy, duct-to-mucosa
anastomosis, is constructed with an inner layer of interrupted 5-0 Vicryl
suture and an outer layer of interrupted 3-0 PDS suture.
Approximately 10cm distal to the pancreaticojejunostomy, the hepat-
icojejunostomy is performed. e surgeon stands on the patient’s right with
instruments and camera in the right-most trocars. is setup allows sewing
toward the surgeon as would be done in an open approach. e end-to-side
hepaticojejunostomy is constructed with a single layer of interrupted (duct
size≤6mm) or running (duct size>6mm) 5-0 Vicryl suture.
An antecolic end-to-side duodenojejunostomy is constructed approxi-
mately 40cm distal to the hepaticojejunostomy, using two layers of running
3-0 Vicryl suture.
A single, 5-mm round, closed-suction drain is brought through the
right abdominal wall and positioned posterior to the hepaticojejunostomy
and anterior to the pancreaticojejunostomy. e trocars are removed under
direct vision and the skin incisions closed with a subcuticular 4-0 monola-
ment absorbable suture.
POSTOPERATIVE MANAGEMENT
Postoperative care after MIS pancreatectomy is similar for both distal
pancreatectomy and pancreaticoduodenectomy. e orogastric tube is
removed at the end of the procedure. Patients are started on clear liquids
on the rst postoperative day, and diet is advanced over the next 48 hours.
Pain is controlled with intravenous ketorolac scheduled every 6 hours and
with patient-controlled intravenous administration of morphine. e drain
is removed on postoperative day 4 if drain amylase is low and no other
signs of pancreatic stula are present. Hospital discharge is allowed on or
after the 5th postoperative day if the patient is tolerating a soft diet and is
w
ithout evidence of complication.
Section I / Pancreas94
OUTCOMES
Distal Pancreatectomy
Several large series of minimally invasive distal pancreatectomy have dem-
onstrated the feasibility, safety, and favorable outcomes of this approach.
Adequately powered, randomized controll ed trials of LDP versus open distal
pancreatectomy (ODP) have not been performed, and the assessment of the
outcomes of these two approaches is predominantly limited to retrospective
comparative trials. Recently, a large meta-analysis of 18 studies including
1,814 patients suggested that minimally invasive distal pancreatectomy is
associated with less blood loss, reduced overall and wound-specic compli-
cation rates, and shorter length of hospital stay. Importantly, no dierences
in operative time, margin status, pancreatic stula rates, or mortality were
seen between the two groups.
To further elucidate whether risk factors for operative morbidity dif-
fer between LDP and ODP, Cho and colleagues performed an analysis of
data from nine separate academic centers comparing LDP and ODP. Of
693 patients undergoing distal pancreatectomy (LDP =254, ODP=439),
multivariate analysis demonstrated that BMI ≤ 27, nonadenocarcinoma,
and pancreatic specimen length≤8.5cm had higher rates of stula after
ODP than after LDP. is study identied no preoperatively variables asso-
ciated with the increased risk of pancreatic stula after LDP compared to
ODP. Additionally, no patient cohorts were identied that had higher rates
of postoperative complication for LDP than for ODP.
Laparoscopic Pancreaticoduodenectomy
Gagner and Pomp published the rst report of laparoscopic pancreaticoduo-
denectomy in 1994 and subsequently published a series of 10 patients in 1997.
e conversion rate for this series was 40% and the operative time was long
(8.5 hours). e authors concluded that there were no perceivable advantages
of the MIS approach. Over a decade passed before the rst substantial series
of total laparoscopic pancreaticoduodenectomy (TLPD) was published by
Palanivelu and colleagues. Of 42 patients undergoing TLPD, the indication
was malignancy in 95%. With a mean operative time of 370 minutes, estimated
blood loss of 65 mL, and pancreatic stula rate of 7%, this report not only
established the feasibility but also clearly set a challenge to investigate this
technique further. To date, only six published series have reported more than
50 patients undergoing TLPD and are shown in Table 8.2. While the outcomes
appear comparable to those reported for open approaches, appropriate and
intentional selection bias in these early experiences limits validation of equiv-
alency or potential advantages. Asbun and colleagues recently reported a
retrospective, comparative analysis of laparoscopic and open pancreaticodu-
odenectomy. Patients undergoing the laparoscopic approach had signicantly
less estimated blood loss, fewer transfusions, and shorter length of hospital
stay. No dierences in overall or pancreas-specic complications were seen;
however, operative time was longer for the laparoscopic group. Our institu-
tion has now performed laparoscopic pancreaticoduodenectomy in over 300
patients, and a comparative analysis is forthcoming. We continue to observe
the typical advantages of MIS approaches with TLPD as reported earlier.
Further investigation should be in evaluating the potential impact of laparo-
scopic approaches on the quality-of-life, oncologic, and long-term outcomes.
Robotic-Assisted Laparoscopic Pancreatic Resection
Robotic assistance has been described as a useful adjunct to pure lapa-
roscopic approaches and is currently gaining interest. Several series have
published outcomes of robotic-assisted pancreatic resection. Zureikat and
Chapter 8 / Minimally Invasive Pancreatic Surgery 95
Publication Year No. of Patients Procedure Op Time (Min) EBL (mL) PF (%) DGE (%) LOS (Days) Mortality (%)
Palanivelu 2009 75 TLPD 357 74 7 – 8 1.3
Kendrick 2010 62 TLPD 368 240 18 15 7 1.6
Giulianotti 2010 60 RALPD 421 394 21 5 22 3
Kim 2012 100 TLPD 487 – 6 2 20 1
Asbun 2012 53 TLPD 541 195 10 11 8 6
Zureikat 2013 132 RALPD 527 300 7 – 10 1.5
Total
b
482 453 263 14 9 13 2
a
Includes only series with ≥50 patients and data sufcient for analysis.
b
Weighted averages.
TLPD, total laparoscopic pancreaticoduodenectomy; RALPD, robotic-assisted laparoscopic pancreaticoduodenectomy; EBL, estimated blood loss; PF, pancreatic stula; DGE, delayed gastric emptying;
LOS, length of hospital stay.
Selected Series of Laparoscopic Pancreaticoduodenectomy
a
TABLE
8.2
Section I / Pancreas96
colleagues reported a large single institutional series of robotic pancreatec-
tomy. Of 250 consecutive robotic pancreatic resections, the most common
operations included are pancreaticoduodenectomy (n=132), distal pancre-
atectomy (n=83), central pancreatectomy (n=13), enucleation (n=10), and
total pancreatectomy. In these selected patients, the safety and feasibility
were established with comparable morbidity and mortality rates compared
to those reported for open approaches.
In a comparative study of LDP versus robotic-assisted LDP, Kang and
colleagues reported greater success with spleen preservation with the use
of robotic assistance (56% vs. 5%, P= 0.027). Signicant dierences in the
study group included a younger age and disease indication. Operative time
(349 vs. 258 minutes, P= 0.016) was longer, and cost (USD 8,300 vs. 3,862)
was signicantly higher for the robotic group compared to the laparoscopic
group. e small sample size and patient selection may account for these
ndings. Patients in the robotic-assisted group were also younger and less
likely to have intraductal papillary mucinous neoplasm, where pericystic
inammation is frequently noted.
Reported advantages and disadvantages of the robotic platform are
listed in Table 8.3. Pertinent advantages may include the relative ease of
training and potential avoidance of prerequisite advanced laparoscopic
skills. e purported advantages of a three-dimensional view, added maneu-
verability, and ne motor movement, while enticing, are immeasurable with
regard to their independent eect on outcomes over pure laparoscopic
approaches. Signicant disadvantages of the current robotic systems are the
lack of haptic feedback and the cost of the equipment and its maintenance.
With the feasibility and favorable outcomes of pure laparoscopic
approaches having already been established, additional comparative trials
of robotic compared to open approaches are of questionable value. e per-
tinent questions are whether the addition of robotic assistance improves
outcomes over pure laparoscopic approaches and does the increase cost
justify its use? e current literature lacks any adequately powered, appro-
priately designed trial to address these important questions. Further, the
answers are unlikely to be forthcoming for the most complex procedures
such as pancreaticoduodenectomy due to the fact that few centers will be
able to perform both approaches in sucient numbers to allow a meaning-
ful comparison.
At present, the main advantage of robotic assistance appears to be cen-
tered toward the surgeon rather than the patient. Clearly, surgeons without
sucient laparoscopic skills will be more able to perform complex laparo-
scopic procedures using robotic assistance. A more widespread application
of MIS approaches will provide advantages for patients. Another potential
advantage requiring further investigation is the ergonomics of surgeon posi-
tioning, which may reduce surgeon fatigue and chronic injuries compared
to pure laparoscopic approaches.
Advantages Disadvantages
“Intuitive”—replicates open skills Lack of haptic feedback
Increased range of motion Expense (purchase, maintenance)
Fine motor movement Set-up time
Three-dimensional view Surgeon remote from the patient
Surgeon ergonomics Loss of bedside “peripheral” view
Advantages and Disadvantages of Robotic-Assisted Approaches
TABLE
8.3
Chapter 8 / Minimally Invasive Pancreatic Surgery 97
Laparoscopic Approaches to Pancreatic Malignancy
A valid concern among many skeptics of minimally invasive approaches to
pancreatic resection is the ability of these approaches to maintain onco-
logic principles. Given the relative recent application of MIS approaches in
pancreatic malignancy, long-term oncologic outcomes are not available.
Surrogates to assess the quality of the oncologic resection include margin
status, number of lymph nodes resected, and short-term recurrence and
survival.
In a multicenter, retrospective, matched cohort analysis of patients
undergoing laparoscopic versus ODP for adenocarcinoma, Kooby and col-
leagues identied no dierence in oncologic outcomes based on approach.
Specically, margin-negative status (74% vs. 66%, P=0.61), number of lymph
nodes harvested (14 vs. 12, P=0.41), and median survival (16 vs. 16 months,
P=0.71) were similar.
We have recently evaluated the outcomes of open and laparoscopic
pancreaticoduodenectomy at our institution from 2008 through 2013. To
avoid the confounding factors of invasiveness, margin-negative rates, and
survival among various types of malignancy, we evaluated only patients
with pancreatic ductal adenocarcinoma. Of 322 patients undergoing pan-
creaticoduodenectomy specically for pancreatic adenocarcinoma, 108
underwent TLPD and 214 underwent OPD. Operative time (379 vs. 387 min-
utes) and need for major venous resection (13% vs. 22%) were not dierent.
e estimated blood loss and length of hospital stay were less for LPD com-
pared to OPD (492 vs. 867mL, P=<0.001, and 6 v s. 9 days, P=<0.001, respec-
tively). With regard to oncologic outcomes, tumor size, margin- negative
resection, and number of lymph nodes harvested were not dierent.
A signicantly smaller proportion of patients in the TLPD group had
a delay greater than 8 weeks from operation to chemotherapy. Despite
similar rates of margin-negative resection, local disease as the initial site
of recurrence was less common in the TLPD group (15% vs. 27%). While
there was no dierence in overall survival, TLPD patients had a longer
progression-free survival.
Major vascular resection during pancreaticoduodenectomy for pancre-
atic head adenocarcinoma has been described as feasible and safe in open
approaches. Primary objectives of major venous resection are to increase
the number of patients eligible for a potentially curative procedure and to
increase the rate of R0 resections. Until very recently, the need for vascu-
lar resection had been a contraindication for laparoscopic approaches. Our
institution reported an early experience suggesting the feasibility and safety
of laparoscopic major venous resection at the time of pancreaticoduode-
nectomy. More recently, a comparative analysis of laparoscopic and open
pancreaticoduodenectomy with major venous resection demonstrated less
blood loss with comparable graft patency and complication rates for the
laparoscopic approach.
CONCLUSION
Minimally invasive approaches for pancreatic resection are feasible and
safe. Whereas level I evidence is lacking, existing comparative trials suggest
noninferiority and possible advantages for laparoscopic compared to open
approaches for both benign and malignant disease. Consistently reported
advantages include reduced blood loss and shorter length of hospital stay
for most procedures. A more widespread acquisition of advanced laparo-
scopic skills or access to robotic platforms will continue to advance the use
of minimally invasive approaches for pancreatic surgery. Oncologic and
quality of life outcomes are needed to assess value in addition to the typical
Section I / Pancreas98
advantages reported for MIS approaches. Careful scrutiny should continue
to assure appropriate outcomes and early identication of unexpected
complications and to substantiate the perceived advantages of minimally
invasive approaches for pancreatic resection.
Suggested Readings
Asbun HJ, Stauer JA. Laparoscopic vs. open pancreaticoduodenectomy: overall
outcomes and severity of complications using the Accordion Severity Grading
System . J Am Coll Surg 2012;215:810.
Kendrick ML. Laparoscopic and robotic resection for pancreatic cancer. Cancer J
2012;18:571.
Kendrick ML, Sclabus GM. Major venous resection during total laparoscopic pancre-
aticoduodenectomy. HPB (Oxford) 2011;13:454.
Kooby DA, Hawkins WG, Schmidt CM, et al. A multicenter analysis of distal pancre-
atectomy for adenocarcinoma: is laparoscopic resection appropriate. J Am Coll
Surg 2010;210:779.
Venkat R, Edil BH, Schulick RD, et al. Laparoscopic distal pancreatectomy is associ-
ated with less overall morbidity compared to the open technique: a systematic
review and meta-analysis. Ann Surg 2012;255:1048.
Zureikat AH, Moser AJ, Boone BA, et al. 250 robotic pancreatic resections: safety and
feasibility. Ann Surg 2013;258:554.
99
INTRODUCTION
At high-volume centers, the operative mortality after pancreaticoduode-
nectomy (PD) is less than 3%. However, morbidity remains high with an
overall rate of postoperative complications ranging from 30% to 65%. ese
complications can lead to prolonged hospital stays, increased readmission
rates, and greater hospital costs. Moreover, in patients who undergo an
operation for pancreatic cancer, adjuvant chemotherapy is delayed. us, it
is important to minimize the complication rate and, when a complication
occurs, to treat it promptly and eectively. e complications of pancreatic
surgery include pancreatic stula, delayed gastric emptying (DGE), hemor-
rhage, biliary stula, and pancreatic exocrine and endocrine insuciency.
In this section, we will review the diagnosis and treatment of each of these
complications.
PANCREATIC FISTULA
Denition and Incidence
A pancreatic stula is an abnormal communication between the pancreas
and adjacent or distant organs or spaces (internal stula) or the skin (exter-
nal stula). Fistulas comprise amylase-rich exocrine pancreatic secretions,
and external stulas are the most common cause of prolonged morbidity
and mortality associated with pancreatic surgery. After PD, a stula forms
due to impaired healing of the pancreatic anastomosis or, after distal pan-
createctomy, incomplete healing of the cut edge of the pancreas. Fistulas
can also form after middle (segmental) pancreatectomy or enucleations of
tumors, particularly in the latter case if the main pancreatic duct is injured.
Fistulas are arbitrarily described as low output if the volume is less than
200mL/d and high output if it is greater than 200mL/d.
Because of variability in how pancreatic stula has been dened,
there is a wide range of the rate of pancreatic stula formation reported in
the literature. To standardize these discrepancies, the International Study
Group on Pancreatic Fistula (ISGPF) published a consensus denition in
2005. Postoperative pancreatic stula was dened as drain output of any
measurable volume after postoperative day 3 with an amylase content of
at least three times the upper limit of normal in the serum. e ISGPF also
developed a grading system (A, B, or C) based on the clinical impact and
additional complications caused by the stula (Table 9.1). Grade A stulas
pose little or no burden on the patient, while grade C stulas are associated
with signicant morbidity and occasional mortality.
Numerous risk factors contribute to stula development. e most
widely accepted risks include a soft pancreatic texture that does not hold
sutures well for the pancreatic anastomosis in PD or sutures or staples for
remnant closure in distal pancreatectomy, a small pancreatic duct (<3mm
Complications of Pancreatic
Surgery
Timothy R. Donahue and Howard A. Reber
9
Section I / Pancreas100
diameter), poor nutritional status (albumin <3g/dL), and high intraopera-
tive blood loss (>1 L). Pancreatic surgeons have also examined dierent
surgical techniques to avoid stula formation. For PD, the technique used
(e.g., duct to mucosa vs. invagination; routine placement of a pancreatic
duct stent) or location (pancreaticojejunostomy (PJ) vs. gastrojejunostomy)
of the pancreatic anastomosis has been examined. e results of numer-
ous randomized trials and meta-analyses are mixed, with one favoring one
technique or location over the other, or no dierence observed. We rou-
tinely perform a partial invagination technique without the use of stents
and have observed an overall stula rate of less than 15% and a rate of about
7% after PD for pancreatic cancer.
For distal pancreatectomy, the incidence of pancreatic stula ranges
from 15% to 25%. Some studies suggest that the stula rate is decreased with
the use of stapled closure. More recently, there is some evidence that rein-
forced stapled closure, using a Seamguard, may further decrease the rate
of stula development. We routinely use stapled closure and Seamguard
where possible but have found that even the 4.8-mm staples cannot com-
pletely seal a thick pancreas. In that case, the pancreas is transected with
cautery, and a sutured closure of the cut surface is performed with a run-
ning and locking 3-0 Prolene suture and an additional suture (4-0 or 5-0
Prolene) to close the pancreatic duct. e incidence of pancreatic stula is
highest in patients undergoing middle (segmental) pancreatectomy rang-
ing from 20% to 60%. is high incidence is due to the presence of both a
closed pancreas surface toward the head of the pancreas and a pancreati-
cojejunal anastomosis of the distal segment.
Treatment
Pancreatic stulas are associated with increased patient morbidity, hospi-
tal stay and costs, and even occasional death due to sepsis or hemorrhage.
erefore, prompt diagnosis and treatment are essential. Four goals of
treatment will be reviewed. ese include (a) good drainage, (b) treatment
of infection, (c) maintenance of good nutritional status, and (d) correction
of electrolyte imbalances.
Grade A B C
Clinical conditions Well Often well Ill appearing/bad
Specic treatment
a
No Yes/no Yes
US/CT (if obtained) Negative Negative/positive Positive
Persistent drainage
(after 3 wk)
b
No Usually yes Yes
Reoperation No No Yes
Death related to POPF No No Possibly yes
Signs of infections No Yes Yes
Sepsis No No Ye s
Readmission No Yes/no Yes/no
a
Partial (peripheral) or total parenteral nutrition, antibiotics, enteral nutrition, somatostatin analog,
and/or minimally invasive drainage.
b
With or without a drain in situ.
US, ultrasonography; CT, computed tomography scan; POPF, postoperative pancreatic stula.
Taken from Bassi C, Dervenis C, Butturini G, et al. Postoperative pancreatic stula: an international
study group (ISGPF) denition. Surgery 2005;138(1):8–13.
Main Parameters for Postoperative Pancreatic Fistula
Grading
TABLE
9.1