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7. Jain G, Chakravartty S, Patel AG.Spleen-preserving distal pancreatectomy with and without
splenic vessel ligation: a systematic review. HPB (Oxford). 2013;15(6):403–10. https://doi.
org/10.1111/hpb.12003. Epub 2012 Dec 2.
8. Ferrone CR, Konstantinidis IT, Sahani DV, Wargo JA, Fernandez-del Castillo C, Warshaw
AL.Twenty-three years of the Warshaw operation for distal pancreatectomy with preservation of
the spleen. Ann Surg. 2011;253(6):1136–9. https://doi.org/10.1097/SLA.0b013e318212c1e2.
J. Wang et al.
Chapter 26
Minimally Invasive Distal Pancreatectomy
withCeliac Artery Resection
GilbertMurimwa andPatricioM.Polanco
Introduction
Locally advanced tumors with involvement of the celiac axis (CA) were traditionally considered unresectable. Yet, with the advancement of perioperative systemic
chemotherapy and improvements in surgical techniques and perioperative care, distal pancreatectomy (DP) with CA resection (DP-CAR) has become a feasible surgical option for selected patients that meet strict criteria. In fact, the most recent
versions of the National Comprehensive Cancer Network (NCCN) guidelines designate pancreatic neck/body tumors with invasion of the CA as borderline resectable tumors when managed at high-volume centers with expertise in these types of
resections [1]. With the advancement of minimally invasive techniques, this procedure is now performed laparoscopically and robotically in many high-volume centers. This chapter will cover general considerations, perioperative adjuncts, surgical
technique, and outcomes of minimally invasive DP-CAR, also known as a modied
Appleby procedure.
G. Murimwa
Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA
P. M. Polanco (
Division of Surgical Oncology, Department of Surgery, University of Texas Southwestern
Medical Center, Dallas, TX, USA
e-mail: Patricio.Polanco@UTSouthwestern.edu
Switzerland AG 2025
E. P. Ceppa et al. (eds.), The SAGES Manual of Evolving Techniques in
Pancreatic Surgery, https://doi.org/10.1007/978-3-031-78409-5_26
*)
441© The Author(s), under exclusive license to Springer Nature
442
G. Murimwa and P. M. Polanco
Historical Evolution
Lyon Appleby initially proposed the eponymous “Appleby” procedure in 1953
when he described an en bloc total gastrectomy with DP and celiac trunk resection
for locally advanced gastric cancer [2]. Nimura etal. then went on to describe a
modied Appleby procedure for pancreatic adenocarcinoma of the body and tail in
1976 [3]. The initial case reports for the procedure all came out of Japan, with multiple surgeons reporting their experience performing DP with en bloc resection of
the celiac artery during the 1970s and 1980s [4–6]. Mayumi and collaborators
reported the rst case series of six patients receiving DP-CAR in 1997, a procedure
they referred to as an “extended DP” and compared this cohort to 19 patients who
received “standard” DP [7]. Notably, they reported no difference in operative time,
postoperative elevation of liver enzymes, or length of stay, while seeing a survival
benet of DP-CAR over the outcomes of unresectable patients. Since these initial
reports, several other groups have reported larger series of DP-CAR operations that
showed improved perioperative and oncologic outcomes (Table 26.1) [8, 9]. Cho
and collaborators reported one of the rst experiences with and feasibility of a
purely laparoscopic DP-CAR for pancreatic cancer in 2011 [10]. Subsequently,
Zureikat etal. at the University of Pittsburgh reported the rst series of roboticassisted DP-CAR operations with comparable results to the open approach [11].
Over the last decade, several other experienced groups have adopted the minimally
invasive approach for this complex operation.
Table 26.1 Selected relevant series and outcomes of distal pancreatectomy with celiac artery
resection (DP-CAR)
R0
margin
Study Study design Population
Beane etal.
2015 [13]
Nakamura
etal. 2016 [9]
Ocuin etal.
2016 [11]
Yamamoto
etal. 2018 [8]
Klompmaker
etal. 2019
[14]
Truty etal.
2020 [15]
DP distal pancreatectomy, DP-CAR distal pancreatectomy with celiac artery resection
Multicenter
retrospective
Single
institution
retrospective
Single
institution
retrospective
Multicenter
retrospective
Multicenter
retrospective
Single
institution
retrospective
DP/
DP-CAR
DP-CAR 80 92 5 41 31
DP-CAR 30 80 14 35 35
DP/
DP-CAR
DP-CAR 191 60 9.5 27 19
DP-CAR 90 88 10 53 36.2
# of
Patients
172/20 NR 1/10 10/15 NR
323/72 80/67 1/4 28/42 29/18
rate
(%)
Mortality
(%)
Morbidity
(%)
Median
survival
(months)
26 Minimally Invasive Distal Pancreatectomy withCeliac Artery Resection
443
Perioperative andOncologic Outcomes
Perioperative Outcomes
Morbidity and mortality unique to the DP-CAR procedure center around the altered
perfusion of the hepatic parenchyma and stomach that postoperatively rely on
reversed, collateral ow through the gastroduodenal artery (GDA) and right gastric
arteries from the superior mesenteric artery (SMA). As such, avoiding hepatic and
gastric ischemia through pre- and intraoperative assessment of these vessels and
their adequacy is essential. In addition to pancreatectomy-specic complications,
early and delayed hemorrhage, particularly from the CA stump or proximal common hepatic artery (CHA) stump, are feared complications driving patient deaths
within the rst 90days. These complications are far more likely in the setting of
postoperative pancreatic stula, and they encourage surgeons to leave drains [12].
In 2015, Beane et al. sought to characterize the perioperative outcomes for
DP-CAR in the US using the National Surgical Quality Improvement Program database from the American College of Surgeons [13]. Of 822 distal pancreatectomies
performed at 43 US hospitals over a 14-month period, only 2.4% of patients received
a CA resection. Operative time for DP-CAR was 70min longer (207 vs. 276min;
p < 0.01), with a higher rate of postoperative acute kidney injury (1% vs. 10%;
p<0.03) and 30-day mortality (1% vs. 10%; p<0.03) when compared with DP.At
high-volume centers, mortality following pancreatic head resections as well as distal pancreatectomies has fallen to below 2% from historical peaks. However, mortality remains high at experienced, high-volume centers for DP-CAR.
In the largest single-center Japanese series reported by Nakamura etal. involving
80 patients receiving DP-CAR over a 17-year period, the incidence of pancreatic
stula, delayed gastric emptying, and ischemic gastropathy was 58%, 25%, and
29%, respectively. Clavien-Dindo grade 3 complications occurred in 41% of
patients, and 4 of them (5%) experienced in-hospital mortality. The 90-day mortality rate was not reported for this series [9].
In a large, international study that included 20 European centers, one Japanese
center, and two American centers (Johns Hopkins Hospital and at the University of
Pittsburgh), 90-day mortality at high-volume centers (performing a median of 70
pancreatoduodenectomies annually) was 16%. When dening high-volume for
DP-CAR as being a single operation performed a year over a 3-year period,
Klompmaker etal. found that 18% of patients who underwent DP-CAR at lowvolume centers died within 90 days after surgery, compared with only 5.5% of
patients at one of the ve high-volume DP-CAR centers. The authors also found
signicant differences in mortality rates across European, Japanese, and American
institutions (16% vs. 8% vs. 4%), likely related to different patient selection criteria
and more aggressive interventions [14].
Truty etal. reported the largest single-center series of DP-CAR, which included
90 patients over 14 years with pancreatic ductal adenocarcinoma treated at the
Mayo Clinic [15]. In this series, 45% of patients had celiac-only arterial
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G. Murimwa and P. M. Polanco
involvement while the remaining 55% of cases required additional arterial resection
and reconstruction. Only 4% of patients received preoperative arterial embolization,
and 13% of operations were completed laparoscopically. In all, 53% of patients had
grade IIIA or higher complications, and 20% suffered from hepatic ischemia and
18% from gastric ischemia, with 10% requiring emergent gastrectomy. In addition,
18% of patients required reoperation. Grade B/C delayed gastric emptying and
grade B/C postoperative pancreatic stula occurred in roughly one-third of patients
while 20% suffered from grade B/C post-pancreatectomy hemorrhage. The 90-day
mortality in the Mayo Clinic series was 10%, with a decrease to 4% in the last 50
cases. Most of the deaths were associated with liver failure, gastric necrosis, or
bleeding. This highlights the signicant morbidity associated with performing
DP-CAR, even in high-volume centers by experienced hands.
Oncologic Outcomes
The oncologic outcomes of DP-CAR for pancreatic adenocarcinoma in the largest
reported series are summarized in Table26.1. Across this aggregate of heterogeneous populations, institutions, and approaches, R0 resection margins ranged from
60% to 92%, while median overall survival varied from 19 to 35months [9, 13–16].
These R0 resection rates and survival outcomes are comparable to the ones for
cephalic and distal pancreatectomies without vascular resection. In Nakamura’s
series, the R0 resection rate was 92% and the median overall survival was 31%.
Strikingly, 21% of patients were alive at 5years postoperatively, which is an impressive result for pancreatic cancer with borderline resectable/locally advanced features [9].
In a multicenter international study by Klompmaker etal., median overall survival for the resection was 19months with some differences across the Japanese,
European, and American cohorts, whose median overall survival was 20, 16, and
24months, respectively. Some of these differences were likely related to variations
in perioperative and multimodality management, including longer neoadjuvant
therapy regimens at the American centers [14].
In the Mayo Clinic series, the rate of R0 margins was 88% with a median overall
survival of 36months. Survival was signicantly better for patients who received
neoadjuvant chemotherapy (44 vs. 8months). Neoadjuvant chemotherapy use rose
from 13% before 2011 to 96% afterward. Ten percent of patients had a local recurrence of disease, 18% had recurrence in the peritoneum, 25% in distant sites, and
14% in multiple sites. In all, 42% of patients remained alive with no evidence of
disease at the time of analysis [15].
Given the wide timeframe in which patients were treated in the aforementioned
studies, signicant variation in the management of pancreatic cancer would be
expected across early and later periods. These mainly include the increased utilization of adjuvant chemotherapy (single-agent rst and then multi-agent) as well as
the use of neoadjuvant chemotherapy and or chemoradiation, among other
26 Minimally Invasive Distal Pancreatectomy withCeliac Artery Resection
445
treatments. Similarly, advances in imaging modalities, the optimization of surgical
technique, the completion of learning curves, and improvements in perioperative
care have most likely played a role in the improvement of perioperative and longterm oncologic outcomes over time.
Minimally Invasive andRobotic DP-CAR
Minimally invasive surgery (MIS) approaches have now been routinely adopted for
pancreatic resections. Several multi-institutional series, prospective trials, and society guidelines support the use of MIS in pancreatic cancer resections which appears
to have equivalent outcomes to the open approach [17–19]. Moreover, two recent
randomized trials have shown that MIS distal pancreatectomies result in shorter
time to functional recovery, less pain, and less blood loss when compared to the
open approach [20, 21]. It has also been shown that in high-volume centers with
experienced surgeons, MIS pancreatectomies with vascular resections and reconstructions can be performed utilizing the robotic platform [22].
Zureikat etal. reported a 30-case series of their experience with robotic DP-CAR,
comparing 19 open to 11 robotic cases [11]. This University of Pittsburgh group
found no signicant differences in morbidity but saw improvements in operative
time, blood loss, and transfusion requirements in the robotic cohort. Median overall
survival approached 3years for both cohorts. In the large international series mentioned above, 15% of DP-CAR procedures were performed using an MIS approach.
Although laparoscopic DP and splenectomy have been increasingly adopted as
the standard of care for left-sided pancreatic body and tail tumors, the technical
complexity of DP with celiac artery resection demands a higher level of expertise
and skill. The technical limitations of the laparoscopic approach for some complex
pancreatic resections have been highlighted, with vascular resections resulting in a
much higher level of conversions [23, 24]. In robotic surgery, the added benets of
three-dimensional stereotactic vision, tremor attenuation, optical magnication, a
higher degree of articulation, and improved ergonomics make it the approach of
choice for high-volume hepatobiliary surgeons with robotic experience who seek to
perform DP-CAR and other complex pancreas operations in a minimally invasive way.
The ultimate decision on what approach to use in a complex operation like
DP-CAR relies on the experience of the surgeon and the surgical team. We strongly
advise against attempting complex pancreas operations robotically if the surgeon is
in the early phases of their pancreas surgery experience or have not achieved robotic
skills prociency. Having disclosed that and for the purpose of the current SAGESHPB Surgery Manual, the following sections describe our perioperative management, preoperative planning, and technique considerations for
robotic-assisted DP-CAR.
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G. Murimwa and P. M. Polanco
Neoadjuvant Therapy
“Biology is the king, case selection is the queen, and the technical maneuvers undertaken are the princes and princesses of the realm” [25]. Due to the high morbidity,
increased perioperative mortality, and limited chance of durable cure, patient selection is paramount before proceeding with DP-CAR.Patients with pancreatic cancer
should be managed in a multidisciplinary fashion and their cases discussed by tumor
boards, ensuring the use of guideline-concordant treatments [1]. To select for patient
“biology,” most centers utilize extended courses of neoadjuvant chemotherapy with
or without radiation therapy. There are compelling data regarding the use of neoadjuvant treatments for pancreatic adenocarcinoma of all stages [26, 27]. This is particularly true for patients with locally advanced tumors where the chances of early
systemic disease and locoregional recurrence are higher than for localized pancreatic cancer [28, 29]. In the USA, most institutions recommend multi-agent therapy
with FOLFIRINOX (5-uoracil, irinotecan, and oxaliplatin) or gemcitabine and
nab-paclitaxel for 3–6 months (or more) before committing the patient to a
DP-CAR.Treatment response is monitored by a drop in CA 19-9 levels and evidence of stable disease or response on imaging and a lack of systemic progression.
Different thresholds for CA 19-9 declines (30–50%) and even the normalization of
CA 19-9 levels have been proposed as prerequisites before proceeding with an intervention [14, 30]. In our institution, we favor a 50% drop of CA 19-9 and normalization. It is important to acknowledge that 6–22% of patients with pancreatic cancer
could have normal levels or are non-secretors of CA 19-9 [31]. Some of these
patients may have elevation of serum CEA levels; therefore, baseline serum testing
is recommended [1].
Preoperative Assessment forDP-CAR
In addition to the standard preoperative assessment, careful patient selection criteria
and anatomic delineation are necessary for surgical planning [16, 32, 33].
Our patient selection criteria include:
• Adequate performance status (ECOG 0–1)
• No major atherosclerotic vascular disease (predominantly in the SMA territory)
• Adequate nutritional status
• No current use of high dose of steroids
• Absence of distant metastatic lesions
• Absence of other prohibitive chronic medical conditions (e.g., Child-Pugh C cir-
rhosis, severe chronic pulmonary disease with high oxygen needs, major cardio-
myopathy with low ejection fraction, etc.)
• Good response to neoadjuvant therapy dened as a decline in CA 19-9 levels or
stable or improved tumor involvement in cross-sectional imaging
26 Minimally Invasive Distal Pancreatectomy withCeliac Artery Resection
For anatomic delineation and surgical planning, high-quality CT chest images
are obtained (to rule out lung metastases) as CT or MRI images of the abdomen and
pelvis with a multiphasic pancreas protocol (arterial and portal venous phase). A
dedicated CT arteriogram is rarely needed but sometimes can be useful to better
characterize abnormal anatomic variants.
With this imaging we specically assess for:
• The presence of variant vascular anatomy such as an accessory right hepatic
artery, replaced right hepatic artery, totally replaced CHA, and accessory left
hepatic arteries, among other anatomic variations. The presence of accessory or
replaced hepatic vessels could favor feasibility of celiac artery resection without
compromising liver perfusion.
• Tumor involvement of the aorta and the most proximal aspect of the celiac artery.
• Tumor involvement of the GDA or proper hepatic artery (PHA).
• Tumor involvement of the portal vein, superior mesenteric vein (SMV), and
splenic vein.
• Overall tumor extension to peripancreatic structures besides the vascular
structures.
In our experience, tumor involvement of the GDA, PHA, and aorta are contraindications for DP-CAR unless arterial revascularization (an aorto-hepatic bypass) is
planned for PHA involvement.
447
Preoperative Adjuncts
Preoperative Coiling
Preoperative coiling of the CHA and at times the CA is performed at some centers
prior to DP-CAR [14]. This procedure is thought to improve collateral ow to the
liver and stomach, reducing rates of postoperative ischemia [14]. Proponents of this
approach argue this also allows preoperative assessment of collateral ow and
avoids futile operations [34–36]. There is no clear evidence for the effectiveness of
preoperative embolization of the CHA for DP-CAR.When coiling is performed, the
coils should be placed by an experienced interventional radiologist, making sure to
leave sufcient space between coil in the CHA and the takeoff of the GDA.
Aortic Stenting
Trabulsi etal. have proposed a novel method, performed in two patients, in which
an endovascular aortic stent is placed to cover the CA at 3weeks prior to denitive
DP-CAR [37]. They hypothesize that this allows the formation of adequate
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G. Murimwa and P. M. Polanco
collaterals preoperatively, minimizing the risk of hepatic or gastric ischemia. While
fascinating, this approach has yet to be widely adopted.
Robotic DP-CAR Surgical Technique
This section will describe our standard approach for robotic DP-CAR procedures.
Variations in set-up, technique, and approach are expected based on the surgeon’s
preferences and expertise. While different types of combined arterial and venous
resections/reconstructions (primary anastomosis, grafts, or others) are occasionally
necessary in cases with more advanced disease, these will not be discussed in this
chapter, since we recommend the open surgical approach for them.
Positioning
After general endotracheal intubation, the patient is placed in a supine French position on a split-leg table over an anti-slip pad that has adequate cushioning for all
pressure points of the back and extremities. Straps or tape across the chest and legs
are placed to prevent sliding of the patient during position changes. The abdomen is
widely prepped and draped using sterile technique. After the ports are inserted, the
patient is placed in 14–16° in a reverse Trendelenburg position with 6–7° of rightsided tilt (see Fig.26.1).
Fig. 26.1 Patient in supine
position with split-leg table
and both arms tucked.
After trocar placement the
patient is positioned in 14°
of reverse Trendelenburg
and 6–7° of right tilt
26 Minimally Invasive Distal Pancreatectomy withCeliac Artery Resection
449
Port Placement
We start by placing a 5mm optical trocar in the left upper quadrant. This is later
exchanged for an 8mm robotic trocar. We complete a thorough diagnostic laparoscopy to rule out peritoneal metastasis. A second trocar (8mm robotic) can be placed
to assist with diagnostic laparoscopy or to perform peritoneal biopsies.
Once peritoneal disease is ruled out, we place the remainder of our trocars. Our
standard approach is to place four robotic trocars of 8mm across the upper abdomen, two assistant ports in the lower abdomen (8mm for the AirSeal insufation
system and 15mm for a utility port), and a right-sided 5-mm port for the “snake”
liver retractor. Figure 26.2 depicts our preferred approach for trocar placement.
Once trocars are in place, we position the patient as described above and dock the
robotic arms. For our standard DP-CAR using the da Vinci Xi system (Intuitive
Surgical), we use the following instruments: fenestrated bipolar forceps (arm 1,
right abdomen), a camera (arm 2, umbilicus), a robotic hook cautery/vessel sealer
(arm 3, mid-left abdomen), and Cadiere forceps (arm 4, left lateral abdomen).
Surgical Steps
1. Division of gastrocolic ligament and mobilization of the greater curvature of
the stomach
We start the procedure by dividing the gastrocolic ligament (bursa) and
exposing the lesser sac. This is followed by division of the short gastric vessels
with the laparoscopic or robotic vessel sealer and cephalad traction of the stomach and left liver with a snake/auto-static liver retractor. Special attention is
given to preserving the right gastroepiploic artery and right gastric arteries to
minimize the chances of gastric ischemia. If invasion of the portal vein by tumor
is anticipated, mobilization of the hepatic exure of the colon and the Kocher
Fig. 26.2 Trocar placement for robotic distal pancreatectomy with celiac axis resection