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Файл:Ординатура / Хирургия / Библиотека им академика М.И. Перельмана / Книга_775_Библиотеки_им_академика_М_И_Перельмана.pdf
Distal Pancreatectomy withEn Bloc
CHA
Celiac Axis Resection
SatoshiHirano, ToruNakamura, andToshimichiAsano
47
Abstract
Distal pancreatectomy with en bloc celiac axis resection
(DP-CAR), which is an extended surgical procedure for
locally advanced cancer of the pancreatic body, is performed for complete resection of tumors with invasion to
the celiac, and/or the common hepatic artery, and/or their
plexuses. Although the procedure of DP-CAR is technically demanding, a high rate of negative surgical margin
resection can be achieved with cautious selection of candidates and with appropriate systematic techniques. A
relatively high morbidity rate due to postoperative pancreatic stula and ischemic gastropathy has been reported.
A recent report on the long-term outcomes following
DP-CAR in 80 patients has described a 5-year overall survival (OS) rate of 32.7% and median survival time of
30.9months. It was revealed that OS for the patients who
underwent preoperative therapy were signicantly better
than for those who underwent upfront surgery.
47.1 Concepts ofDistal Pancreatectomy
withCeliac Axis Resection (DP-CAR)
Locally advanced cancer of the body of the pancreas often
involves the common hepatic artery (CHA) and/or the celiac
axis (CA), with perineural invasion of the nerve plexuses
surrounding these arteries. Although these tumors are
regarded as borderline resectable or locally advanced diseases according to the NCCN guidelines® Version 1.2021
[1], distal pancreatectomy with celiac axis resection
(DP-CAR) may be the only surgical option for treatment of
such advanced diseases [2]. An advantage of DP-CAR is
reduction in the likelihood of a positive retroperitoneal mar-
S. Hirano (*) · T. Nakamura · T. Asano
Department of Gastroenterological Surgery II, Hokkaido
University Faculty of Medicine, Sapporo, Japan
e-mail: satto@med.hokudai.ac.jp
gin by complete en bloc resection of the distal pancreas,
together with the entire surrounding structures, especially
the CHA, CA, and the circumferential nerve plexus along
with the superior mesenteric artery (SMA), without the need
for either arterial, pancreatobiliary or gastrointestinal reconstruction (Fig.47.1).
This procedure was originally designed as en bloc lymphadenectomy combined with total gastrectomy and resection
of the celiac axis for advanced gastric cancer by Appleby in
1953 [3]. It was rst adopted by Nimura in 1976 [4] for
patients with advanced pancreatic body cancer with invasion
of the celiac axis. A modication to the procedure with preservation of the entire stomach was made by Ogata and his
colleagues [5] in 1991 (in Japanese with English abstract)
and Kondo [6] in 2001, which resulted in better postoperative nutritional status. The rst report regarding the long- term
outcome of DP-CAR was published by Kondo and Hirano in
2007 [7], which included the results of 24 consecutive
patients with favorable postoperative survival. Since then,
the procedure and the term “DP-CAR” have been widely
SA
PV
Pl CA
Du
kidney
Fig. 47.1 Schematic cross-sectional view demonstrating the resection
area of distal pancreatectomy with en bloc celiac axis resection
(DP-CAR). The dotted line indicates the dissection plane. adr adrenal
gland, Ao aorta, CA celiac axis, CHA common hepatic artery, crus crus
of the diaphragm, Du duodenum, g celiac ganglion, IVC inferior vena
cava, pl celiac plexus, PV portal vein, SA splenic artery, SV splenic vein
IVC
g
crus
Ao
crus
SV
g
adr
spleen
kidney
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022
M. Makuuchi et al. (eds.), The IASGO Textbook of Multi-Disciplinary Management of Hepato-Pancreato-Biliary Diseases,
https://doi.org/10.1007/978-981-19-0063-1_47
361
362
CA
S. Hirano et al.
acknowledged. Nowadays, several pancreatic surgeons have
performed this procedure for carcinoma of the body and tail
of the pancreas.
47.2 Resected andPreserved Organs
inDP-CAR
Perineural invasion in patients with pancreatic body cancer
can spread towards the celiac plexus and ganglions directly
or via the nerve plexuses surrounding the splenic and the
common hepatic arteries. Although DP-CAR includes en
bloc resection of these arteries and plexuses, reconstruction
of the arterial system is not required because of early development of a collateral arterial circulation via the pancreatoduodenal arcades from the superior mesenteric artery. The
entire alimentary tract, including the stomach and bile duct,
which are not invaded by the cancer, is preserved.
Cholecystectomy is, however, performed for preventing
postoperative ischemic rupture of the gallbladder. If the
tumor of the pancreatic body invades other organs directly,
concomitant resection of the organs, including the alimentary tract, could be performed. In case that a tumor has
invaded the stomach to a depth that necessitates full- thickness
resection, total gastrectomy should be considered because
healing of the anastomosis might be disturbed by an insufcient collateral arterial ow. As far as possible, the entire
stomach should be preserved in cases without cancer invasion of the stomach, to maintain the patient’s nutritional status and tolerance of oral anticancer agents. SMA preservation,
even with complete eradication of the surrounding plexus, is
the key feature of this procedure, which maintains arterial
supply to the hepatobiliary system and the stomach.
Resection of the portal vein is an optional procedure.
47.3 Arterial Supply totheLiver
andtheStomach After DP-CAR
After division of the CA with the CHA and splenic artery
(SA), the hepatic and the gastric arterial ow depend on the
ow from the gastroduodenal artery (GDA), which should,
therefore, denitely be preserved with the pancreatic head
during DP-CAR.The collateral pathways via the SMA, pancreatoduodenal arcades, and GDA maintain the arterial blood
supply to the hepatobiliary system. Since the collateral pathways also ensure arterial ow to the right gastroepiploic
artery, the entire stomach can be preserved (Fig.47.2).
In the past, preoperative coil embolization of the CHA
had routinely performed to enlarge the collateral arterial
pathway, so as to reduce ischemia-related complications
such as ischemic gastropathy, liver abscess, and perforation
of the biliary system. However, the usefulness of the CHA
PHA
CHA
GEA
GDA
PPD
APD
Fig. 47.2 Schematic drawing of collateral arterial pathways via the
pancreatoduodenal arcades from the superior mesenteric artery following DP-CAR.The arrows show the direction of arterial ow from the
superior mesenteric artery to the liver and stomach via the pancreatoduodenal arcades. APD anterior pancreatoduodenal arcade, CA celiac
axis, CHA common hepatic artery, GDA gastroduodenal artery, GEA
right gastroepiploic artery, LGA left gastric artery, PHA proper hepatic
artery, PPD posterior pancreatoduodenal arcade, SA splenic artery,
SMA superior mesenteric artery
LGA
SA
TUMOR
SMA
embolization has been reported to be negative [8]. The procedure has been no longer essential.
47.4 Selection ofCandidates forDP-CAR
Tumor progression is cautiously evaluated mainly with preoperative multi-detector row computed tomography (MDCT), with supplemental use of magnetic resonance imaging
(MRI) and endoscopic ultrasonography (EUS). The indication for DP-CAR is locally advanced ductal adenocarcinoma
of the body of the pancreas, such as that involving or abutting
the CHA, the root of the SA, and/or the CA, without involvement of the GDA, SMA, and inferior pancreatoduodenal
artery (IPDA). Patients with involvement of less than approximately half the circumference of the SMA plexus should be
considered candidates for DP-CAR because complete dissection of the SMA plexus without exposing the cancer can
be achieved by dividing the plexus on the opposite side of the
tumor. For oncologically safe ligation and division of the
root of the CA in front of the aorta, a 5–7mm non-cancerous
length of the CA from the adventitia of the aorta is required.
47.5 Surgical Procedure ofDP-CAR
DP-CAR usually includes resection of the distal pancreas
and the spleen, together with en bloc resection of the celiac,
common hepatic and left gastric arteries, the celiac plexus
47 Distal Pancreatectomy withEn Bloc Celiac Axis Resection
CHA stump
crus
CA stump
363
CA
GDA
Pancreatic
stump
Fig. 47.3 Post-resection view during distal pancreatectomy with en
bloc celiac axis resection (DP-CAR). Ao aorta, CA celiac axis, CHA
common hepatic artery, crus crus of the diaphragm, GDA gastroduodenal artery, graft interposed iliac vein graft, IVC inferior vena cava, RV
renal vein, SMA superior mesenteric artery, SMV superior mesenteric
vein
graft
SMV
SMA
Ao
Kidney
O/P
and bilateral ganglions, and the circumferential nerve plexus
around the SMA. Left perirenal fat tissue, the left adrenal
gland, the entire retroperitoneal fat tissue containing lymph
nodes cranial to the left renal vein, the transverse mesocolon
covering the body of the pancreas, and the inferior mesenteric vein are also resected (Fig.47.3).
To achieve R0 resection, a systematic procedure of
DP-CAR, which consisted of right and left dorsal (rst step),
ventral (second step), and medial (third step) approaches, is
recommended (Fig.47.4). In the rst step (dorsal approach),
the lower parts of the SMA are exposed following Kocher’s
maneuver, with complete eradication of the right celiac ganglion by exposing the right crus of the diaphragm. The plexus
of the SMA is rst divided at the dorsal end (opposite side of
the tumor), and the excision is extended by 4–5cm in the
longitudinal direction. The median arcuate ligament has to
be divided to expose just the root of the CA where it should
be divided. Then, after moving to the left side, en bloc resection of the retroperitoneal fat, together with the upper part of
the perirenal fat, including the left adrenal gland cranial to
the left renal vessels are performed in exposing the left crus.
In this approach, bilateral para-aortic nodes and ganglions
are completely dissected. In the second step (ventral
approach), transection of the pancreas is performed after
dividing the common hepatic artery. When a tumor is located
near the GDA, it should be mobilized laterally in order to
obtain a cancer-free margin at the site of division of the pancreatic parenchyma. Reconstruction of the portal and/or
superior mesenteric vein should be performed in this step, if
necessary. In the third step (medial approach), division of the
SMA plexus that was performed in the rst step is extended
longitudinally to just proximal to the IPDA to achieve complete resection of the plexus. The procedure is completed
2
3
SMA
1
Fig. 47.4 A systematic procedure for achieving negative surgical mar-
gin in DP-CAR.The procedure is composed with 3 steps; the rst step
(①) is Rt. and Lt. dorsal approach, the second (②) is ventral approach,
and nal step (③) is medial approach
1
after dissecting between the SMA plexus and the uncinate
process of the pancreas.
Accidental injury to the IPDA or GDA compromises collateral blood ow and leads to fatal complications, such as
gastric necrosis and/or liver infarction. If this occurs, microscopic anastomosis between the proper hepatic artery and
middle colic artery (MCA) [9], or the right gastroepiploic
artery and MCA [10] could be a possible option for maintaining arterial ow to both the stomach and the liver.
47.6 Postoperative Course Following
DP-CAR
The most frequent morbidity after DP-CAR is pancreatic stula, which occurs relatively easily because the pancreatic
parenchyma needs to be divided at the pancreatic head in
patients with a tumor extending to the proximal end of the
pancreas, beyond the portal vein. In such cases, the cut surface of the pancreas becomes wider than that after usual distal pancreatectomy, in which the pancreatic parenchyma is
divided at the neck of the pancreas. It is rather important to
insert an indwelling drain at an appropriate position beside
the pancreatic stump during surgery, so as to avoid postoperative hemorrhage from a pseudoaneurysm in the stump of
the CHA.The second most common morbidity is ischemic
gastropathy due to decreased gastric blood ow [11].
According to data from 80 consecutive patients who underwent DP-CAR [12], the major complications dened as
364
S. Hirano et al.
grade 3 or higher in the Clavien-Dindo classication occurred
in 33 (41.3%) patients; pancreatic stula and ischemic gastropathy occurred in 47 (57.5%) and 23 (28.8%) patients,
respectively. Four patients out of 80 (5%) died in the hospital. Postoperative hospital stays ranged from 12 to 208days,
with a median of 38days [12].
One of the other postoperative complications is stubborn
diarrhea due to complete dissection of the nerve system
around the SMA, CA, and bilateral ganglions. From a published data, approximately half of the patients regularly
required anti-diarrheal agents, and the remaining half only
occasionally required or never used the agents over a median
follow-up period of 39months [13].
Contrary to the adverse effects of resection of nerve tissues, patients enjoy the complete disappearance of pain, even
if it has been controlled by opioids just before surgery [6].
Since both the incidence of morbidity and poor quality of
life postoperatively are major factors inuencing the tolerance of adjuvant treatment, surgeons should make greater
efforts to improve these factors following DP-CAR.
47.7 Long-Term Outcomes Following
DP-CAR
In 2007, the long-term outcomes of DP-CAR were rst
reported in a series of 23 patients with locally advanced
pancreatic body cancer who underwent DP-CAR under a
policy of “surgery rst” [7]. With R0 resectability in 91%
of the cases and a median follow-up time of 27.4months,
the estimated 5-year survival rate was 42% and the median
survival was 21months. Nine years after the rst report, a
recent report that included 80 patients was published from
the same institute, which indicated estimated disease-specic 1-, 3-, and 5-year overall survival rates of 81.1%,
56.9%, and 32.7%, respectively, and a median survival time
of 30.9 months after a median follow-up period of
63.5months [12].
Despite the excellent local control with an R0 resection
rate of 92.5% in the report, early recurrence (predominantly
in the liver) occurred after surgery, which resulted in poor
survival time. It was also revealed that the survival time of
the patients who underwent preoperative therapy were signicantly better than for those who underwent upfront surgery [12]. The ndings show DP-CAR should be performed
as part of multidisciplinary treatment.
Although DP-CAR could be used to treat locally advanced
pancreatic body cancer, future prospective studies with a
large patient cohort for ensuring adequate patient selection,
and perioperative treatments are necessary to demonstrate
the effectiveness of this innovative surgery.
References
1. NCCN Clinical Practice Guidelines in Oncology (NCCN
Guidelines
www.nccn.org/professionals/physician_gls/pdf/pancreatic.pdf
2. Kondo S, Katoh S, Hirano S, Ambo Y, Tanaka E, Okushiba S,
Morikawa T, Kanai M, Yano T. Results of radical distal pancreatectomy with en bloc resection of the celiac artery for locally
advanced cancer of the pancreatic body. Langenbeck Arch Surg.
2003;388:101–6.
3. Appleby LH.The coeliac axis in the expansion of the operation for
gastric carcinoma. Cancer. 1953;6:707.
4. Nimura Y, Hattori T, Miura K, Nakajima N, Hibi M.A case of
advanced carcinoma of the body and tail of the pancreas resected
by the Appleby operation. Operation. 1976;30:885–9. (In Japanese)
5. Hishinuma S, Ogata Y, Matsui J, Ozawa I, Inada T, Shimizu H,
Kobu K, Ikeda T, Koyama Y.Two cases of cancer of the pancreatic
body undergoing preservation with distal pancreatectomy combined with resection of the celiac axis. Jap J Gastroenterol Surg.
1991;24:2782–6. (In Japanese with English abstract)
6. Kondo S, Katoh H, Omi M, Hirano S, Ambo Y, Tanaka E, Okushiba
S, Morikawa T, Kanai M, Yano T. Radical distal pancreatectomy
with en bloc resection of the celiac artery, plexus, and ganglions
for advanced cancer of the pancreatic body: a preliminary report on
perfect pain relief. JOP. 2001;2:93–7.
7. Hirano S, Kondo S, Hara T, Ambo Y, Tanaka E, Shichinohe T,
Suzuki O, Hazama K.Distal pancreatectomy with en bloc celiac
axis resection for locally advanced pancreatic body cancer: longterm results. Ann Surg. 2007;246:46–51.
8. Ueda A, Sakai N, Yoshitomi H, Furukawa K, Takayashiki T, Kuboki
S, Takano S, Suzuki D, Kagawa S, Mishima T, Nakadai E, Miyazaki
M, Ohtsuka M. Is hepatic artery coil embolization useful in distal pancreatectomy with en bloc celiac axis resection for locally
advanced pancreatic cancer? World J Surg Oncol. 2019;17:124.
9. Suzuki H, Hosouchi Y, Sasaki S, Araki K, Kubo N, Watanabe A,
Kuwano H.Reconstruction of the hepatic artery with the middle
colic artery is feasible in distal pancreatectomy with celiac axis
resection: a case report. World J Gastrointest Surg. 2013;5:224–8.
10. Kondo S, Ambo Y, Katoh H, Hirano S, Tanaka E, Okushiba S,
Morikawa T, Igawa H, Yamamoto Y, Sugihara T. Middle colic
artery-gastroepiploic artery bypass for compromised collateral
ow in distal pancreatectomy with celiac artery resection. HepatoGastroenterology. 2003;50:305–7.
11. Kondo S, Katho H, Hirano S, Ambo Y, Tanaka E, Maeyama Y,
Morikawa T, Okushiba S.Ischemic gastropathy after distal pancreatectomy with celiac axis resection. Surg Today. 2004;34:337–40.
12. Nakamura T, Hirano S, Noji T, Asano T, Okamura K, Tsuchikawa
T, Murakami S, Kurashima Y, Ebihara Y, Nakanishi Y, Tanaka K,
Shichinohe T.Distal pancreatectomy with en bloc celiac axis resection (modied Appleby procedure) for locally advanced pancreatic
body cancer: a single-center review of 80 consecutive patients. Ann
Surg Oncol. 2016;23:969–75.
13. Hirano S, Kondo S, Tanaka E, Shichinohe T, Tsuchikawa T, Kato K,
Matsumoto J.Postoperative bowel function and nutritional status
following distal pancreatectomy with en-bloc celiac axis resection.
Dig Surg. 2010;27:212–6.
®
). Pancreatic adenocarcinoma version 1. 2021. https://
Modified Distal Pancreatectomy
withCeliac Axis En-bloc Resection
Ken-ichiOkada andHirokiYamaue
48
Abstract
Since most pancreatic adenocarcinomas recur systemically, and tumor involving arterial structures recur rapidly
even after the radical resection. In the era of neoadjuvant
therapy, surgeon should re-consider whether the presence
of just an R0 resection should be the primary issue of cure
in borderline resectable and locally advanced pancreatic
adenocarcinoma. By safer modication of the Appleby
operation, this procedure attract the attention of pancreatic surgeon again as a radical pancreatectomy for borderline resectable or locally advanced pancreatic body/tail
carcinoma. The roles of the Appleby operation and arterial resection are the ability to take a wide surgical margin
in pancreatic body/tail carcinoma, and to relieve the cancer pain by celiac axis en-bloc resection combined with
removal of the tumor inltrating nerve plexuses. The
modied Appleby operation, a synonym for “distal pancreatectomy with celiac axis en-bloc resection”; DP-CAR
was feasible and safe compared with standard distal pancreatectomy when it was performed at high-volume center. In the era of stronger regimen of chemotherapy for
pancreatic carcinoma, there will be increased frequency
of the chance to consider the indication of this procedure.
The procedure may be justied in highly selected patients
owing to the potential survival benet in sophisticated
institutions. In this chapter, we particularly describe about
the technique and impact of preservation of the left gastric
artery in DP-CAR.
48.1 Introduction
The application of distal pancreatectomy with celiac axis enbloc resection; DP-CAR [1], so-called the modied Appleby
operation, for pancreatic carcinoma still remains controversial because of the lack of large number of study. One of the
advantages of this procedure is the surgical radicality of deep
dissection behind of tumor by the division of the root of the
celiac axis, and another is the impact to resolve the preoperative cancer pain according to the tumor invasion into nerve
plexus. There are surely several prior reports suggesting that
an R0 resection is an essential requirement for long survival.
In contrast, an R0 resection is not the only consideration for
the impact of survival in advanced pancreatic carcinoma.
Recently, in an international multicenter analysis for 174
patients with pancreatic ductal adenocarcinoma who underwent DP-CAR, the R0 resection rate was 60%, neoadjuvant
and adjuvant therapies were applied for respectively 69%
and 67% of the patients, and the median overall survival
period was 19months [2]. Despite these reports, the indications for DP-CAR remain controversial with regard to the
curability and survival benet. This procedure can provide a
clinical benet for the patients with borderline resectable or
locally advanced pancreatic body/tail carcinoma after the
strategy of neoadjuvant therapy. Furthermore stronger and
adequate preoperative therapy prior to surgery is required to
improve their survival.
48.2 History, Background,
andModication ofAppleby
Operation forPancreatic Cancer
In 1973, Fortner introduced the regional resection of pancreatic cancer with major vascular en-bloc resection as a new
K.-i. Okada (*) · H. Yamaue
Second Department of Surgery, Wakayama Medical University,
Wakayama, Japan
e-mail: okada@wakayama-med.ac.jp
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2022
M. Makuuchi et al. (eds.), The IASGO Textbook of Multi-Disciplinary Management of Hepato-Pancreato-Biliary Diseases,
https://doi.org/10.1007/978-981-19-0063-1_48
approach [3]. In this literature, actual survival by KaplanMeier estimate was 62% at one year, compared with a 36%
one year survival rate for 17 patients undergoing pancreati-
365
366
Type IIa(4.5%) Type IIb(5%)
K.-i. Okada and H. Yamaue
coduodenectomy for less advanced cancer at same institution
from 1959–1969 [4]. This approach was described that the
greatest potential benet of regional pancreatectomy would
appear to be in patients with a small pancreatic cancer where
regional resection would give a wide margin. Appleby operation was rstly reported as resection of celiac axis for complete lymphadenectomy in radical resection of gastric
carcinoma in 1953 [5, 6]. Nimura etal. reported the adaptation the Appleby operation for resection of pancreatic body/
tail carcinoma involving celiac axis and/or common hepatic
artery in 1976 [7]. In 1991, Hishinuma etal. modied this
procedure with preservation of the entire stomach, which
improved postoperative nutritional status and quality of life
[8]. Konishi et al. reported reconstruction of the hepatic
artery when pulsation in the proper hepatic artery was weak
after test occlusion of the celiac axis in 2000 [9]. Since then,
several institutions have reported their experienced with the
modied Appleby operation for advanced pancreatic body/
tail carcinoma, i.e., distal pancreatectomy combined with
celiac axis en-bloc resection, which was named DP-CAR by
Kondo etal. [10]. Despite reports of a few long-term survivors, the overall survival benet and the risks of this challenging operation are unknown because previous reports
have included only a small number of patients. In the era of
safer modication and innovation of the Appleby operation
and the transition of the concept of borderline resectable
pancreatic carcinoma, this procedure attract pancreatic surgeon’s attention again as a radical pancreatectomy for borderline resectable or locally advanced pancreatic body/tail
carcinoma. In 2014, we have rstly introduced the preservation of the left gastric artery (LGA) on the basis of anatomical features in DP-CAR (modied DP-CAR) [11].
48.3 The Anatomical Features About Celiac
Trunk andIts Branches
Although there are many reports on the classication of
celiac artery anatomy, the classication that can be applied to
variations of past papers is relatively simple and easy to
understand is the classication described by Marco-Clement
etal. in 2016 (Fig.48.1) [12]. In this paper, almost 90% are
Type I called complete celiac trunk, Type Ia: complete bifurcated celiac trunk (LGA arises rst) is 57.6%, Type Ib: complete trifurcated celiac trunk is 32.1%, and incomplete celiac
trunk is the Type IIa called hepatosplenic trunk is Type IIa
CHA
CHA
LGA
CA
SA
CHA
Type Ia(57.6%) Type Ib(32.1%) Type Ic(0.8%)
LGA
CA
SA
CHA
CA
CA
LGA
SA
SA
LGA
Ex. Br
CHA
CA
LGA
SA
Fig. 48.1 Classication of celiac branches by Marco-Clement etal. [12]
48 Modied Distal Pancreatectomy withCeliac Axis En-bloc Resection
367
4.5%, and the gastrosplenic trunk Type IIb is 5%. From the
viewpoint of anatomical factors, LGA cannot preserved in
Type Ib cannot preserve in pancreatic body cancer with positive invasion of the roots of the celiac artery, common hepatic
artery, and splenic artery. For other are examined for each
individual case, and the LGA can be preserved without
microscopic cancer residual (R0). The planned surgical
method and planned dissection layer should be planned in
consideration of the distance from the tumor to the LGA and
the site of the LGA root [11].
48.4 The Organs andTissues Resected by
theModied Appleby Operation
(DP-CAR)
Hirano and Kondo etal. described [1] the resected organ and
tissues by this procedure were as follows, the procedures
routinely included en bloc resection of the celiac, common
hepatic, and LGA, the celiac plexus and ganglions, the nerve
plexus around the superior mesenteric artery, a part of the
crus of the diaphragm and the Gerota’s fascia, the left adrenal gland, the retroperitoneal fat tissues bearing lymph nodes
above the left renal vein, the transverse mesocolon covering
the body of the pancreas, and the inferior mesenteric vein.
Resection of the portal vein and the middle colic vessels was
optional. In general, no reconstruction of the arterial system
was required because of early development of the collateral
arterial pathways via the pancreatoduodenal arcades from
the superior mesenteric artery. In addition, with preservation
of the stomach, no reconstruction of the alimentary tract was
required. Sato etal. reported about the feasibility of middle
colic artery—LGA bypass in patients who undergo LGA
resecting DP-CAR [13]. Based on the anatomical features
and the relationship between the tumor and artery, the LGA
and inferior phrenic arteries can be preserved. Table 48.1
shows the list of organs, vessels, and other tissues which is
resected and preserved in this procedure.
48.5 The Indication ofModied Appleby
Operation (DP-CAR) inPatient
withPancreatic Body/Tail Carcinoma
First, this procedure should be performed in the selected
institutions where well-trained and skillful staffs [2].
Regarding the tumor status, in the early period of the adaptation of the modied Appleby operation (DP-CAR), this
procedure was indicated for patients with pancreatic body/
tail carcinoma involving celiac axis and/or common hepatic
artery. Recent literature reported this procedure is indicated
for the patients whose pancreatic body/tail tumors involved
or touched at least one of the common hepatic artery, the
root of the splenic artery, or the celiac axis [1], which means
Table 48.1 The organs, vessels, and other tissues that are resected or
preserved in the modied Appleby operation
Resection Preservation
Organ Pncreas (body/tail),
Vessels Celiac artery,
Other
tissues
a
Several institutions resect gallbladder, left gastric artery routinely, and
others preserve under denite condition or reconstruct it
left adrenal gland,
gallbladder
common hepatic
artery, splenic
artery, dorsal
pancreatic artery,
short gastric
vessels, posterior
gastric artery,
inferior mesenteric
vein.
Part of the crus of
the diaphragm, the
Gerota’s fascia, the
celiac plexus and
ganglions, the
nerve plexus
around the superior
mesenteric artery,
the retroperitoneal
fat tissues bearing
lymph nodes above
the left renal vein,
the transverse
mesocolon
covering the body
of the pancreas.
a
, spleen
Stomach, duodenum
inferior
pancreaticoduodenal
artery, gastroduodenal
artery
(pancreatoduodenal
arcades), proper
hepatic artery, the right
gastric and right
gastroepiploic vessels,
gastrocolic trunk.
Right adrenal gland,
bilateral kidneys.
Optional
resection
Portal vein,
middle colic
vessels. Left
gastric
a
artery
and
inferior
phrenic
arteries can
be preserved
based on the
anatomical
features.
a parts of resectable pancreatic body/tail carcinomas situated near the root of the splenic artery also indicated for this
procedure as well. Our investigation regarding the relationship between curability and the distance between the edge
of the tumor and the splenic artery root in patients who
underwent standard DP revealed that the microscopically
positive margins were detected more frequently in the
patients with tumors situated ≤10 mm from the splenic
artery than those with a distance of >10mm from the splenic
artery [14]. Therefore, we suggest that DP-CAR should be
performed to obtain an R0 resection in those patients with
potentially resectable pancreatic body/tail carcinoma who
would otherwise receive a standard DP.In addition to that,
our study demonstrated the overall survival rate in patients
with pathologically negative invasion for portal venous system and artery (double negative invasion) was greater than
that of the other patients. Moreover, extended pancreatectomy with major arterial resection did not result in any longterm survivors in many previous reports. Therefore, we
evaluate carefully the patients with double negative invasion
into portal venous system and artery on preoperative imaging study for indication of DP-CAR.
368
K.-i. Okada and H. Yamaue
48.6 Risk Score fortheModied Appleby
Operation (DP-CAR)
From an international multicenter analysis for 191 DP-CAR
patients, the 90-day mortality rate was 5.5% at 5 high- volume
(≥1 DP-CAR/year) and 18% at 18 low-volume DP-CAR
centers (P=0.015). A risk score with age, sex, body mass
index, American Society of Anesthesiologists score, multivisceral resection, open versus minimally invasive surgery,
and low- versus high-volume center performed well in both
the design and validation cohorts (P=0.642). The main nding is that annual DP-CAR case volume is the most important predictor for 90-day mortality. The investigators of this
study concluded that future studies should aim at (prospectively) validating the clinical risk score, which was made
available online at www.pancreascalculator.com [2].
48.7 Preoperative Preparation
fortheModied Appleby Operation
(DP-CAR)
The necessity of the preoperative coil embolization still
remains controversial. Several investigators have performed
the modied Appleby operation without preoperative coil
embolization of the common hepatic artery (CHA). The
safety and efcacy is still needed to be evaluated in the clinical trials. Although, there is no evidence of decreased risk of
these ischemia related complication by preoperative embolization of the CHA, preoperative angiography should be carried out and variations of the inferior pancreaticoduodenal
artery (IPDA) were examined to safely perform this
procedure. The preoperative coil embolization of the CHA
should be performed as collaborative work between the surgeons and the interventional radiologist. The surgeons should
request the planned ligation/division site precisely to them,
and the radiologist was requested to place the coil in hopeful
position without coil migration into the preserving planned
arteries in a safe manner. The diameter of the IPDA usually
increase about 1.5–2 times by the procedure.
the proper hepatic artery (PHA). Conrming the negative for
cancer cell inltration of frozen section by harvesting the
periarterial nerve plexus around the bifurcation should be
performed to evaluate the resectability in patients whose
tumor is adjacent this region. Kocher’s maneuver should be
performed in case of accidental bleeding from portal venous
system. The gastrocolic trunk was preserved for venous
return from the stomach. Transection of the pancreas was
performed with enough margin from the tumor to conrm
the negative for cancer cell inltration. In patient whose
tumor involves the portal vein, the resection and reconstruction of the portal vein was performed antecedently. After
pancreatic transaction, the dissection of the retroperitoneum
must be performed from the right side to the left side in the
manner of radical antegrade modular pancreatosplenectomy
procedure, because the surgical eld of this procedure is better and safer for surgeon and assistant in case of accidental
bleeding. By en-bloc dissecting the lymph nodes around the
CHA, the right celiac ganglion and celiac nerve plexus, the
origin of the celiac axis was exposed. Then, blood ow
through the PHA, the right gastric artery, and the right gastroepiploic artery was conrmed by palpation, and intrahepatic arterial ow was also checked by intraoperative Doppler
ultrasonography after clamping the end of the CHA in the
patients who had undergone preoperative embolization of
the CHA.The CHA was divided just proximal to the origin
of the GDA.In the cases with dog-leg branching of PHA and
GDA, great care was taken to preserve both arteries by avoiding the ligation of bifurcation site. Lifting up the cut end of
the distal pancreas and the CHA into the left caudal side, the
superior mesenteric artery (SMA) was dissected from the
surrounding lymph node and nerve plexus toward its origin.
Great care was taken to preserve the inferior pancreaticoduodenal artery (IPDA) arising from the SMA or the rst jejunal
artery. The dissecting layer around the SMA is connected to
that of the celiac axis (CA) from the caudal side to dorsal
side. The origin of the celiac axis was identied circumferentially just above the aorta and as divided. The origin and the
direction of inferior phrenic arteries should be taken care in
dissecting around the CA in front of the aorta.
48.8 The Procedure andPitfalls
ofModied Appleby Operation
(DP-CAR)
The specic procedure for DP-CAR was as follows: rstly,
right gastroepiploic artery/vein, right gastric artery/vein are
encircled by vessel tape and preserved. Before the transection of the neck of the pancreas, rstly the bifurcation of the
gastroduodenal artery (GDA) and the common hepatic artery
(CHA) was exposed, followed by exposure of the origin of
48.9 Preservation oftheLeft Gastric Artery
ontheBasis ofAnatomical Features
Despite the recent favorable surgical outcomes, delayed gastric emptying (DGE) or ischemic gastropathy after the modied Appleby operation (DP-CAR) is a continuous and
frustrating complication. DGE induced by ischemic gastropathy, with had an incidence varying from 13.0% to 30.8% in
previous series [1, 14], is not a life-threatening complication,
but results in a prolonged hospital stay and leads to a
ab
48 Modied Distal Pancreatectomy withCeliac Axis En-bloc Resection
369
decreased quality of life (QOL), poorer nutritional status and
delayed administration of postoperative adjuvant chemotherapy. In the past studies, several patients underwent combined
total gastrectomy to prevent gastric ischemic complications
during the modied Appleby operation (DP-CAR) [1, 14].
The left gastric artery (LGA) develops as the rst branch of
the celiac trunk embryologically, and it was reported to
branch antecedently in 68% to 72% of cases as a rst branch
of trifurcation described as above [12]. However, the procedures used for the modied Appleby operation (DP-CAR)
routinely included en-bloc resection of the LGA [1], although
pancreas body cancer requiring DP-CAR does not always
involve the LGA or the nerve plexus surrounding the
LGA. We prospectively tried to preserve the LGA with
enough margins in patients whose LGA branched antecedently and in whom the distance between the LGA and carcinoma was more than 10 mm to clarify whether LGA
preservation in DP-CAR (modied DP-CAR) could reduce
the incidence of DGE and other postoperative complications
[11] (Fig. 48.2). The medical records of 37 consecutive
patients who underwent DP-CAR were evaluated for the
incidence of DGE in 23 patients (62%) with LGA-resecting
DP-CAR (conventional DP-CAR) and compared it with 14
patients (38%) who underwent distal pancreatectomy with
resection of the common hepatic artery and splenic artery,
with preservation of the LGA (modied DP-CAR) for pan-
creatic carcinoma. The patients with tumors situated more
than 10 mm away from the antecedent branching LGA
underwent modied DP-CAR.The antecedent branching of
the LGA was found in 19 patients (51%) in this study. In the
conventional DP-CAR group, the LGA were involved in 20
patients (87.0%). Clinically relevant DGE according to the
ISGPS grades were: 30% in the conventional DP-CAR
group, and 0% in the modied DP-CAR group (P=0.035).
The R0 rate was higher in the modied DP-CAR group
(79%) compared to the conventional DP-CAR group (43%)
(P=0.048). Multivariate analysis demonstrated that resection of the LGA was an independent risk factor for increased
incidence of DGE. Therefore, modied DP-CAR signicantly reduced the incidence of DGE in comparison to conventional DP-CAR. In this series, distal stomach blood/
nerve supply including right gastric, right gastroepiploic
arteries and antral nerve branch were preserved, but proximal stomach blood supply including, left gastroepiploic
and short gastric arteries were resected in all cases. The
LGA preservation can reduced the ischemic gastropathy
after DP-CAR, and this approach (preservation of the LGA
when feasible) provides another option for surgeons performing DP-CAR.Furthermore, in patients whose collateral ow had injured or proved to be insufcient during the
surgery, arterial reconstruction would compromise collateral ow [13].
T
T
Fig. 48.2 The patients with tumors situated more than 10mm away
from the antecedent branching left gastric artery (LGA) underwent
modied DP-CAR. A schematic drawing showing the relationship
between the division site and the branching site of the LGA (a) in conventional DP-CAR and (b) in distal pancreatectomy with resection of
the common hepatic and splenic artery, with preservation of the LGA
(modied DP-CAR). Double-headed arrows indicating the site of the
division. CA celiac axis, SA splenic artery, CHA common hepatic artery,
LGA left gastric artery, T tumor
370
K.-i. Okada and H. Yamaue
48.10 Surgical Technique Preserving Left Gastric Artery
Even when we intent to preserve left gastric artery (LGA) preoperatively, right gastroepiploic artery/vein, right gastric
artery/vein are also rstly encircled by vessel tape and preserved, and we rule out the cancer cell inltration into the periarterial nerve plexuses around GDA or CHA as soon as
possible to evaluate resectability. We check the pulsation of
GDA and PHA before clamping. After clamping the CHA, we
conrmed the pulsation again, and the CHA was ligated and
divided at the distal part described as above. We encircled the
LGA by vessel tape to preserve in the early phase of surgery as
a destination of dissection. Lifting up the CHA by en-bloc dissecting of lymph nodes around the CHA from the pancreas,
the celiac axis was exposed. After conrming that the patients
were negative for cancer cell inltration into the nerve plexus
surrounding the LGA by an intraoperative histopathological
diagnosis of several frozen sections, the celiac artery was
divided just after the branching of the LGA.The resection and
reconstruction of the portal vein is performed antecedently
before radical antegrade modular pancreatosplenectomy procedure. The depth of dissecting layer of retroperitoneum was
controlled with wide margin according to the tumor position.
Figure48.3 shows the surgical eld after modied DP-CAR.
48.11 Postoperative Complications After
Modied Appleby Operation
(DP-CAR)
The rates of morbidity after this procedure is not low [2]. The
presence of postoperative hemorrhage from the resected stump
of the common hepatic artery due to a pancreatic stula after
ST
DP-CAR is difcult to rescue by interventional radiology
(IVR) techniques because of the resection of the common
hepatic artery. In addition, DP-CAR is associated with signicant morbidities such as ischemic gastropathy or hepatic ischemia [15]. Total gastrectomy was added if severe ischemia of
the stomach was observed during operation and if surgeon
could not exclude the possibility of future necrosis of the remnant stomach in several institutions. Unplanned arterial reconstruction was required in patients with accidental injury [1].
The possible ischemic gastropathy includes irregular, shallow,
and wide ulcerations usually in cardia of the stomach thought
to be ischemic in origin and delayed gastric emptying after
surgery. The issue would directly affect the postoperative
recovery and the schedule of adjuvant chemotherapy. As
regarding the hepatic ischemia, the recent studies reported the
low incidence of clinically relevant hepatic infarction as a case
requiring drainage of abscess, and usually abnormal liver
function recovered after several days. Necrotic cholecystitis is
also reported which could occur postoperatively probably due
to the spasm of the gastroduodenal artery and/or proper hepatic
artery reported in several studies. The most concern is diarrhea
after the removal of the plexus around the celiac axis and the
superior mesenteric artery, because the diarrhea would inuence the nutritional status and quality of life after surgery. In
many studies, diarrhea after this procedure is reported as controllable degree to maintain quality of life and nutritional status by medication, usually with loperamide hydrochloride,
and rarely with tincture of opium [1].
48.12 Conclusions
The modied Appleby operation (DP-CAR) may be justied
in highly selected patients owing to the potential survival
benet compared with patients without resection, and these
patients should be treated in multimodal therapy. Recent
additional modication by preservation of LGA, i.e. “modied DP-CAR” can lead the procedure to be a safer option.
Stump of CHA
LGA
CA
PV
GDA
RGEAV
Fig. 48.3 The surgical eld after modied DP-CAR. ST stomach, PV
portal vein, SMV superior mesenteric vein, SV splenic vein, RGEAV
right gastroepiploic artery/vein, GDA gastroduodenal artery, CA celiac
artery, LGA left gastric artery, SMA superior mesenteric artery, CHA,
common hepatic artery
SV
SMV
SMA
References
1. Hirano S, Kondo S, Hara T, etal. Distal pancreatectomy with en
bloc celiac axis resection for locally advanced pancreatic body cancer: long-term results. Ann Surg. 2007;246:46–51.
2. Klompmaker S, Peters NA, van Hilst J, etal. Outcomes and risk
score for Distal Pancreatectomy with Celiac Axis Resection
(DP-CAR): an international multicenter analysis. Ann Surg Oncol.
2019;26:772–81.
3. Fortner JG.Regional resection of cancer of the pancreas: a new
surgical approach. Surgery. 1973;73:307–20.
4. Fortner JG, Kim DK, Cubilla A, etal. Regional pancreatectomy: en
bloc pancreatic, portal vein and lymph node resection. Ann Surg.
1977;186:42–50.
5. Appleby LH.The coeliac axis in the expansion of the operation for
gastric carcinoma. Cancer. 1953;6:704–7.