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326 J.L. Miller-Ocuin et al.
tumor board. Curative intent treatment options offered to this patient included
preoperative chemotherapy on or off protocol versus surgery upfront followed by
adjuvant chemotherapy. Our patient chose to enroll in UPCI protocol 13-074 (two
cycles of gemcitabine/nab-paclitaxel with or without the autophagy inhibitor
hydroxychloroquine). He completed therapy and underwent repeat staging
contrast-enhanced CT of the chest, abdomen, and pelvis, which demonstrated no
distant disease and a stable primary. He had a favorable biochemical response, with
CA19-9 decreasing to 28.1 [10]. Therefore, decision was made to proceed with
robotic-assisted pancreaticoduodenectomy (PD).
Technical Pearls of Robotic-Assisted Pancreaticoduodenectomy
• Entry into lesser sac and mobilization of right colon
• Kocher maneuver and opening of ligament of Treitz
• Jejunal and gastric transection
• Portal dissection
– Remove common hepatic artery node
– Identify and ligate GDA
– Identify suprapancreatic portal vein and begin tunnel
– Portal lymphadenectomy and transection of bile duct
• Infrapancreatic SMV dissection and completion of the retropancreatic
tunnel
• Division of the pancreas
• Uncinate dissection and specimen retrieval
• Cholecystectomy (if gallbladder present)
• Reconstruction.
Management
Pancreatic cancer is fundamentally a systemic disease in a majority of the patients at
the time of diagnosis. This requires the clinician to integrate the timing of local
control with the systemic management of this disease. The traditional sequencing of
surgery followed by chemotherapy has proven inadequate despite dramatic
improvements in mortality following the PD over the last 30 years, and morbidity
of the open operation remains high. This high morbidity following the traditional
open PD limits receipt of critical systemic chemotherapy that is required to improve
survival. Several groups have demonstrated that postoperative complications affect
ability to receive critical systemic chemotherapy with nearly 48% of subjects in one
25 Robotic Approaches to the Patient with Pancreatic Adenocarcinoma 327
study never progressing to adjuvant therapy [4, 14]. There are several approaches to
circumvent this clinical dilemma. First, it has been demonstrated that reversing the
sequencing of surgery and chemotherapy results in more subjects receiving both
modalities [15]. Second, we can reduce the morbidity of the surgery through the use
of minimally invasive surgical (MIS) approaches. At our institution, we follow an
innovative and aggressive algorithm in a majority of patients that favors administration of newer, more effective systemic chemotherapies preoperatively, followed
by MIS PD and subsequent adjuvant chemotherapy. One additional potential
benefit to this approach is that we are able to tailor the adjuvant chemotherapy
based on the histopathologic response to the preoperative regimen.
Robotic Pancreaticoduodenectomy
Our institution utilizes seven ports for robotic-assisted pancreaticoduodenectomy,
including a 10-mm camera port, three robotic arms, a 5-mm liver retractor, and two
assistant ports. Port placement configuration is depicted in Fig. 25.2. Following
abdominal access and insufflation, the abdomen is inspected for metastatic disease.
Provided none is found, we proceed with mobilization, the first few steps of which
can be performed laparoscopically or with robotic assistance. The patient is positioned in steep reverse Trendelenburg. We first enter the lesser sac through the
gastrocolic ligament and continue dissection laterally to fully mobilize the right
colon, exposing the duodenum. Next, a Kocher maneuver is performed to the level
of the left renal vein, taking all the retroperitoneal attachments off of the pancreas
and exposing the medial and inferior borders of the superior mesenteric artery
(SMA). The ligament of Treitz is opened, allowing the proximal jejunum to be
pulled u nderneath the SMA. The jejunum is transected with an endovascular stapler, and the mesentery is divided with a bipolar vessel sealer (LigaSure) at the
border of the mesentery and serosa, completing the Kocher maneuver and linearizing the duodenum. We then divide the greater omentum at the level of the
gastric antrum, and the right gastroepiploic artery is taken with the LigaSure. The
lesser omentum is opened and the stomach is transected with an endovascular
stapler. One unique aspect of the robotic PD is the inability of the surgeon to
palpate the plain between the uncinate and SMA, as is classically described in the
open approach. The decision of resectability and need for vascular resection must
be appreciated before the operation based on adequate compute tomography. Thus
the sequencing of the robotic PD is slightly different, and the jejeunum and stomach
are divided early.
At this point, the robot is docked, if not already done. With the operating surgeon
at the robotic console and the assisting surgeon positioned at the bedside between the
patient’s legs, the portal structures and retropancreatic tunnel are dissected. The
common hepatic artery (CHA) is exposed by identification and removal of the CHA
lymph node. CHA exposure is continued until the right gastric and gastroduodenal
arteries (GDA) are exposed (Fig. 25.3a). CHA flow is confirmed on ultrasound by
328 J.L. Miller-Ocuin et al.
Fig. 25.2 Standard port placement for robotic-assisted pancreaticoduodenectomy. The peritoneum is accessed with a 5 mm optical viewing trochar using a 0° laparoscope in the left upper
quadrant. This port is later exchanged for an 8 mm robotic port for Arm 1. The camera should be
placed approximately 2 cm to the right and 2 cm above the umbilicus, to align with the SMV and
optimize visualization of the uncinate dissection. Port placement can be moved up or down
depending on the distance from the xiphoid process to the umbilicus (up for longer distance, down
for shorter distance). The assistant ports should be placed approximately halfway between the
camera and R2 (RLQ) and R1 (LLQ), respectively. The LLQ port site serves as the extraction site,
and is converted to a GelPort following removal of the specimen
Doppler and color flow after vessel-loop facilitated occlusion of the GDA prior to
GDA ligation. The suprapancreatic portal vein is identified at the apex of the triangle
formed by the common hepatic artery, GDA, and superior border of the pancreas.
The avascular plane is developed in a cephalad-to-caudad direction, thereby
beginning the retropancreatic tunnel from above. We then identify the common bile
duct (CBD), and all lymphatic tissue lateral and posterior to it is cleared inferiorly
toward the specimen. An aberrant or replaced right hepatic artery, if present, will be
identified posterior to the CBD, and should be dissected circumferentially and traced
proximally toward the SMA. The CBD is transected with an endovascular stapler, as
we have found that this minimizes bile spillage that is difficult to evacuate during the
uncinate dissection (alternatively a bulldog clamp can be placed.) The peritoneum
overlying the inferior border of the pancreas is opened, and dissection is carried
down until the infrapancreatic SMV is identified. The retropancreatic tunnel is
25 Robotic Approaches to the Patient with Pancreatic Adenocarcinoma 329
completed (Fig. 25.3b) and the pancreas is transected with electrocautery; “cold”
transection is reserved for the duct.
After the pancreas is divided, attention is turned to dissecting the retroperitoneal
margin and uncinate process. Special attention is given to the recurrent uncinated
arterial and venous branches off of the SMA and SMV, as they are easily evulsed
and can be a source of major intraoperative blood loss. Cephalad, we identify
individually ligate the superior pancreaticoduodenal vein. The final resection bed is
depicted in Fig. 25.3c. If the gallbladder is in situ, a cholecystectomy is performed
at this point. The specimen is retrieved through the left lower quadrant assistant
port, which must be enlarged. Pneumoperitoneum is reestablished with placement
of a GelPort.
330 J.L. Miller-Ocuin et al.
b Fig. 25.3 Robotic-assisted pancreaticoduodenectomy. a Detailed view of portal dissection. The
gastroduodenal artery (1) is isolated for ligation, typically via a vascular stapler and the stump is
further reinforced with a clip. The common hepatic artery (2) and portal vein (3) can also be
identified. The common bile duct (4) will also be transected using a stapler. b Creation of the
retropancreatic tunnel. Dissection proceeds along the inferior and superior borders of the pancreas,
at the level of the pancreatic neck, and allows for creation of a tunnel beneath the pancreas and
above the mesenteric vasculature. c Completed pancreaticoduodenectomy resection view. Left
panel with retraction of the superior mesenteric vein, shows careful dissection and removal of all
the perivascular tissue along the plane of Leriche, clearing the superior mesenteric artery (1) and
portal vein (1) margins. Right panel shows the dissected portal vein margin (2), the gastroduodenal
artery stump (3), which is reinforced with a surgical clip, the cut edge of the pancreas (4), with a
readily identifiable pancreatic duct, and the divided common bile duct (5). d Creation of
pancreaticojejunostomy in modified Blumgart technique. The jejunum (1) is approximated to the
pancreatic parenchyma (2) with 2-0 silk horizontal mattress sutures through the seromuscular layer
of jejunum. Electrocautery is utilized to create a small enterotomy in the jejunum. Then, a
duct-to-mucosa pancreaticojejunostomy is created using 5-0 PDS sutures over a Hobbs pancreatic
stent (Hobbs Medical, Inc., Stafford Springs, CT, USA) to ensure duct patency. Finally, the
anterior layer is created using 2-0 silk sutures to approximate the seromuscular layer of the
jejunum to the pancreatic parenchyma. e Creation of the choledochojejunostomy. The common
hepatic duct (1) is sutured to the jejunum (2) using interrupted absorbable 5-0 sutures for small
ducts with or without a stent, or running 4-0 V-LOC suture (Covidien, New Haven, CT, USA) for
larger, thicker ducts (shown here)
The enteric reconstruction is then carried out with meticulous attention, as most
morbidity and mortality of PD is attributed to anastomotic leakage and failure. First
a duct-to-mucosa modified-Blumgart pancreaticojejunostomy technique is performed (Fig. 25.3d), typically over a pancreatic duct stent [16]. We typically use 3
2-0 silk for the transpancreatic/seromuscular sutures, with the middle suture
straddling the pancreatic duct. Once tied in place, an enterotomy is created, and we
use 5-0 polydiaxanone for the duct-to-mucosa anastomosis. The anterior seromuscular layer is then placed. The bilio-enteric anastomosis is constructed, either
by interrupted or continuous suture technique, depending on duct size; a running
technique is employed for larger, thicker bile ducts, and an interrupted technique is
used for smaller, softer ducts (Fig. 25.3e). Third, the gastrojejunostomy is performed by a stapled technique and sutured closure of the common enterotomy is
done in two layers. Alternatively a “handsewn” gastrojejunostomy (or duodenojejunostomy) in a two-layered fashion can be formed. Following creation of the
anastomoses, a 19 French closed suction, round, fluted surgical drain is placed
anterior to the pancreaticojejunostomy and the hepaticojejunostomy, but posterior
to the gastrojejunostomy. The falciform ligament is used to create a pedicled tissue
flap to cover the GDA stump, which is marked with a 10 mm clip in case postoperative angiography is needed [17]. Unanticipated vascular involvement of the
superior mesenteric vein or portal vein can be resected for an R0 resection due to
the precision, control, and dexterity afforded by the robotic platform. We do not
typically leave a nasogastric tube, as there is no evidence to support its routine use.
Postoperative care is focused on early diet advancement as tolerated, and conservative intravenous fluid management, titrated to hemodynamic parameters, and
urine output through a modified enhanced recovery after surgery (ERAS) pathway.
25 Robotic Approaches to the Patient with Pancreatic Adenocarcinoma 331
The ICU is not routinely used. We use a modified Verona protocol [18] to manage
the operative drain. Serum and drain amylase are measured on POD1 and POD3.
If POD 1 amylase is less than 5000 and decreas es by POD 3 in a clinically stable
patient, the drain is removed on POD3.
Following robotic-assisted pancreaticoduodenectomy, our patient was discharged home on postoperative day 5 after an uneventful recovery. Final pathology
demonstrated a poorly differentiated adenocarcinoma with Evans Grade IIB treatment [19] effect, positive for perineural invasion without definitive lymphovascular
invasion, 0/65 lymph nodes positive for metastases, and negative (R0) resection
margins.
Alternative Approaches and Controversies
• Open pancreaticoduodenectomy
– Higher morbidity
• Fully laparoscopic pancreaticoduodenectomy
– Steeper learning curve
– Less easily disseminated.
Perioperative Outcomes Following Robotic PD
In 2006, one of the largest series of open PD to date was reported by Johns
Hopkins, with 1,432 cases for pancreatic malignancies. Winter et al. reported a
mean operative time of 380 min, a mean blood loss of 800 mL, mean length of stay
of 9 days, 58% R0 resections, 5% pancreatic fistula rate (pre-ISPFG criteria), and a
2% mortality rate [20]. This impressive study provides a metric for comparison of
outcomes when describing a new technical platform such as robotic-assisted PD.
Similar to the adoption of laparoscopic PD, early reports of robotic PD began
with smal l case series; Giulianotti performed and reported the first series in 2003
[21]. Over time, experiences grew, leading to larger series. Data suggested similar
oncologic outcomes, decreased blood loss, increased operative time, and increased
cost (Table 25.1). A recent review of studies published before 2012 evaluated five
series of robotic PD, including 131 patients; the (weighted) mean operative time
was 510 min and complications occurred in 38.9% of patients, including 26%
postoperative pancreatic fistula and 2.3% mortality [22].
The University of Pittsburgh reported the institution’s first 250 consecutive
robotic resections; 132 of these were RPD. With a conversion rate of 8% (4.5 in the
last 112 cases), the review demonstrated a median estimated blood loss of 300 mL,
332 J.L. Miller-Ocuin et al.
30-day mortality
(%)
LOS
(days)
POPF
(%)
Lymph nodes harvested
(n)
R0 resection
(%)
EBL
(mL)
Time
(min)
Patients
(n)
2010 50 568 394 90 18 38 22 8
published
Buchs [30] 2011 44 444 387 90.9 16.8 18 13 4.5
Guilianotti
Author Year
Table 25.1 Peri-operative outcomes of robotic-assisted pancreaticoduodenectomy
Chan [31] 2011 8 478 200 . . 33.3 12 0
[29]
2012 30 476 485 100 13.2 6.7 9.8 3.3
Zureikat [23] 2011 24 512 320 . . 21 9 4.2
Chalikonda
Lai [33] 2012 20 492 247 73 10 35 13.7 0
Zureikat [34] 2013 132 527 300 87.7 19 17 10 1.5
Bao [35] 2014 28 431 100 63 15 29 7.4 7
[32]
Baker [36] 2015 22 22 454 97.8 . 4.6 7 0
Chen [37] 2015 60 410 400 97.8 13.6 13.3 20 1.7
POPF Postoperative pancreatic fistula
25 Robotic Approaches to the Patient with Pancreatic Adenocarcinoma 333
mean length of stay of 10 days, 7.4% pancreatic leak (grade B and C) by ISGPF
criteria, and a 1.5 and 3.8% 30- and 90-day mortality rate, respectively [23].
More recently, larger series of robotic PD are being reported. Additionally, some
studies include matched comparisons to open PD. We have performed a contemporary cohort-matched multicenter comparison of perioperative outcomes of
robotic PD and open PD that demonstrated reduced blood loss (mean difference = 181 mL, P = 0.04) and reduced major complications (OR = 0.64,
P = 0.003) despite increased operative times (mean difference = 75.4 min,
P = 0.01). Furthermore, the approaches were equivalent in terms of oncologic
outcomes, with similar margin status and lymphadenectomy [24].
Our patient received 5 months, or five cycles, of adjuvant gemcitabine and
nab-paclitaxel. He remains free of radiographic or biochemical evidence 24 months
after surgery.
Adjuvant Therapy
As previously discussed, we believe that one of the principle impediments to
improving survival in PDA over the last three decades is the significant morbidity
of the pancreaticoduodenectomy, which often precludes administration of systemic
chemotherapy [4]. Kendrick et al. have demonstrated that the minimally invasive
approach can mitigate this morbidity and lead to more subjects receiving systemic
chemotherapy. In this study 12% open patients undergoing open resection were
delayed in receiving, or did not receive, adjuvant therapy versus 5% of totally
laparoscopic pancreaticoduodectomy [25]. We see similar results in our own
experience. A retrospective review of 463 patients at our institution demonstrates
increased administration of adjuvant chemotherapy in the robotic approach versus
open approach (82% vs. 70%; p < 0.017). Furthermore, robotic PD was an independent predictor of decreased complications (OR 0.47; p = 0.011) and increased
adjuvant chemotherapy (OR 2.24; p = 0.012). Patients who received adjuvant
chemotherapy had a longer OS compared to those who did not (31 vs. 13 months;
p < 0.0001); patient receiving 6 cycles had a median OS of 39 months
(p < 0.0001) (submitted for publication).
Posttreatment Surveillance and Interval Staging
Our current approach is to perform triple-phase CT scan, serum Ca 19-9, and
physical exam every 6 months for 2 years and then yearly thereafter up to 10 years.
Tzeng et al. compared five follow-up strategi es—no scheduled follow-up as
“baseline” and four increasing strategy groups with escalating utilization of CA
19-9, clinical examination, and imaging—and demonstrated that increased frequency and intensity of follow-up measures increases costs without any associated
survival benefit[26].
334 J.L. Miller-Ocuin et al.
Conclusion
We performed a review of quality metrics of all robotic PD cases performed at our
institution, and determined that continuous assessmen t of quality metrics permitted
safe and feasible implementation of the robotic approach [27]. This study identified
benchmarks to optimize surgeons training in the approach. Subsequently, our
institution has developed a mastery-based robotic simulation curriculum that
combines virtual reality, inanimate object, and biotissue exercises to train surgeons
on the robotic platform ex vivo. Training surgeons then develop skills at the patient
bedside. Finally, trainees are gradually incorporated onto the robotic console in an
increasing complexity of cases.
In order to safely imp lement minimally invasive pancreatic surgery, a structured
training program is needed to allow new generations of surgeons to master skills of
the approach while maintaining the tenets of open surgery. It is prudent to continuously analyze operative parameters, postoperative morbidity and mortality, and
oncologic outcomes, as with any new surgical technology platform [28].
Box 25.3 General Pearls of Pancreaticoduodenectomy for Ductal
Adenocarcinoma
• Good preoperative planning
– Multidisciplinary strategy to maximize chances of receiving systemic
chemotherapy
– High-quality cross-sectional imaging and identification of anatomic
variants (i.e., replaced/aberrant right hepatic artery) and vascular
involvement
• Meticulous surgical technique—major steps should be performed the
same way every time
• Careful attention to the recurrent uncinate vessels and the superior pancreaticoduodenal vein
• Leave an intraoperative drain
• Falciform ligament flap to cover the GDA stump.
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