REVIEW ARTICLE
Left-Sided Pancreatic Cancer
Distal Pancreatectomy and its Variants: Radical Antegrade
Modular Pancreatosplenectomy and Distal Pancreatectomy With
Celiac Axis Resection
Steven M. Strasberg, MD and Ryan Fields, MD
Abstract: Adenocarcinoma of the body and tail of the pancreas is an
aggressive malignancy, and classically there have been few survivors
after surgery. Radical antegrade modular pancreatosplenectomy and
distal pancreatectomy with celiac axis resection are new procedures for these
tumors. Radical antegrade modular pancreatosplenectomy is designed to es-
tablish an operation with oncologic rationales both for the dissection planes
used to achieve negative margins and the extent of node dissection. The ex-
tent of lymph node dissection is based on the descriptions of N1 lymph
node drainage, and dissection planes are based on fascial planes of the
retroperitoneum. Radical antegrade modular pancreatosplenectomy is
modular, adjusting the posterior plane of dissection based on the position of
the tumor on preoperative computed tomograms. It is also performed right
to left to increase visibility and control blood supply early. Radical ante-
grade modular pancreatosplenectomy is not an extended pancreatectomy
but brings the rationales of the modern Whipple procedure to left-sided
tumors. In long-term results from our center in 47 patients, there was a high
negative tangential margin rate of 89% and an actuarial overall 5-year
survival rate of 35.5%. The actual 5-year survival in 23 patients was
30.4%. Distal pancreatectomy with celiac axis resection is a procedure
for cancers that have involved the celiac axis. It is based on the fact that
resection of the celiac axis may be performed without devascularizing
the liver, which then receives its blood supply by the pancreaticoduo-
denal arcade. It is an extended pancreatectomy. Mature long term results
are just becoming available. Results with distal pancreatectomy with
celiac axis resection are mixed with some series reporting few or no
long-term survivors, whereas others report long-term survival at ap-
proximately 20%.
Key Words: Pancreatic cancer, radical antegrade modular
pancreatosplenectomy (RAMPS), distal pancreatectomy with celiac
artery resection (DP-CAR)
(Cancer J 2012;18: 562Y570)
A denocarcinoma of the body and tail of the pancreas is a
highly malignant tumor. Until the past decade, there were
few long-term survivors after surgical resection. For instance, in
1990, it was stated that there were 5 known 5-year survivors with
this disease.1 With advances in detection, staging, and treatment,
especially surgical treatment, a small subset of patients with this
disease is now being cured. This article will focus on radical
antegrade modular pancreatosplenectomy (RAMPS) and distal
From the Section of Hepato-Pancreato-Biliary Surgery, Department of Sur-
gery, the Department of Pathology, and the Alvin J Siteman Cancer
Center, Washington University in St Louis, MO; and Barnes-Jewish
Hospital, St Louis, MO.
Reprints: Steven M. Strasberg, MD, Washington University in Saint Louis,
660 S Euclid Ave, Box 8109, Saint Louis, MO 63110.
E-mail: strasbergs@wustl.edu.
Copyright * 2012 by Lippincott Williams & Wilkins
ISSN: 1528-9117
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pancreatectomy with celiac artery resection (DP-CAR), also
called the Appleby procedure. Radical antegrade modular
pancreatosplenectomy is a promising technique, which has
recently been shown to have a 35% 5-year overall survival
(OS). Distal pancreatectomy with celiac artery resection is an
extended pancreatectomy for lesions that have spread locally
to involve the celiac axis. There have been several reports of
this procedure, and its evaluation is continuing.
RAMPS
History of Left-Sided Pancreatectomy
and Development and Rationale of the
RAMPS Procedure
The rst left-sided pancreatectomies were performed in the
late 19th century2 in Europe. The rst in the United States was
apparently performed by Briggs in St Louis in 1890.3 Until 1999,
the standard operation was performed by early ligation of the
splenic artery followed by mobilization of the spleen and pan-
creas, usually from a left-to-right direction,4 although some authors
performed the mobilization right-to-left.2 Oncologic goals and the
strategies to achieve them, namely, the extent of node dissection and
the dissection planes used to optimize margin negativity, were not
well dened, possibly because most left-sided resections before
1990 were performed for chronic pancreatitis.
Radical antegrade modular pancreatosplenectomy (RAMPS)
has been performed in our center since 1999.5Y7 It was designed to
establish an operation with oncologic rationales both for the dis-
section planes used to achieve negative margins and the extent of
lymph node dissection. The extent of the lymph node dissection is
based on the anatomic descriptions of N1 lymph node drainage
from this part of the pancreas by OMorchoe.8 The anatomic planes
for the posterior margin, which is the one that is most often posi-
tive, are based on the relationship of the fascial planes of the ret-
roperitoneum to the posterior surface of the pancreas as described
by Lei et al.9 The plane of the posterior dissection is modular and
depends on the position of the tumor in relation to the adrenal
gland on preoperative computed tomographic (CT) scans as ex-
plained below. Radical antegrade modular pancreatosplenectomy
is not an extended pancreatic resection. Its intention is to bring
the oncologic rationales of the modern Whipple procedure, i.e., N1
lymph node dissection and dissection with the best chance of
attaining negative margins, to left-sided pancreatectomies.
Anatomic Basis for the RAMPS Procedure
Position and Relations
As described by Lei et al,9 the distal pancreas (pancreatic
body and tail) lies within the pararenal fascial space (pararenal,
meaning near the kidney), that is, behind the peritoneum and in
front of a distinct layer of fascia called the anterior renal fascia
& Volume 18, Number 6, November/December 2012
The Cancer Journal & Volume 18, Number 6, November/December 2012
(Fig. 1)). The kidney and the adrenal lie behind the anterior renal
fascia in the perirenal space (perirenal, meaning around the
kidney), bounded posteriorly by another layer of fascia, the pos-
terior renal fascia. The contents of the perirenal space are contained
in a fatty loose areolar tissue, whereas the connective tissue of the
pararenal space is much more brous in nature. The 2 peritoneal
layers of the mesocolon separate on the anterior surface or inferior
border of the pancreas, one leaf passing upward on the retro-
peritoneum and one downward. This explains why the base of the
mesocolon is frequently involved by pancreatic tumors.
Anteriorly, the stomach is the organ that is most commonly
invaded by left-sided pancreatic cancer because the posterior
parietal peritoneum overlying the pancreas is usually in contact
with the visceral peritoneum covering the posterior wall of the
stomach. Laterally, the spleen is frequently involved by tail
lesions. The structures that share the pararenal space with the
pancreas on its anteroinferior aspect include the duodenum, the
splenic exure of the colon (more laterally), and the root of
the mesocolon as noted earlier. The posterior relationships of
the pancreas are the most important to the surgeon because the
posterior resection margin is the most common site of R1 re-
section. Posteriorly and superiorly pancreatic tumors invade the
splenic artery, the celiac artery, the common hepatic artery, and
sometimes, the origin of the left gastric artery. More posteriorly
and inferiorly, the superior mesenteric artery, the aorta, and the
conuence of the splenic and superior mesenteric veins may be
involved. Pancreatic tumors also invade posteriorly through the
anterior renal fascia to involve the adrenal and less commonly
the kidney or the vasculature of these organs.
The RAMPS procedure attempts to maximize the chance
of getting negative tangential margins by placing the resection
plane behind the anterior renal fascia (anterior RAMPS) when
the tumor has not penetrated the posterior capsule of the pan-
creas on preoperative CT scans, and behind the adrenal gland
and Gerota fascia when it has (posterior RAMPS)5 (Fig. 2). In
each case, the goal is to add an extra margin of safety in re-
secting these tumors, which can spread microscopically beyond
their radiographically visible or palpable margins. In each case,
the adrenal vein is the intraoperative guide to the position of
the margin. In anterior RAMPS, the posterior margin is formed
by identifying the adrenal vein at its junction with the left re-
nal vein and following its anterior surface retrograde in a right-
to-left direction to the left adrenal gland. The posterior margin
continues out on the surface of the adrenal and Gerota fascia.
In the posterior RAMPS, the adrenal vein is divided at its ter-
mination with the renal vein and elevated along with the adrenal
to give the posterior margin.
FIGURE 1. Fascial spaces of the retroperitoneum. A indicates
left adrenal gland; D, duodenum; K, kidney; P, pancreas;
SF, splenic flexure of colon.
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Left-Sided Pancreatectomies: RAMPS and DP-CAR
FIGURE 2. Planes of posterior margin and direction of
dissection in different types of distal pancreatectomies.
Lymph Node Drainage
Both anatomical and pathological studies have been used
to determine the propensity of a cancer to metastasize to spe-
cic lymph nodes. The anatomical approach uses dissection and
injection of markers to identify the primary and secondary nodal
drainage stations from particular organs. Pathological lymph node
mapping studies use specimens obtained at surgery or autopsy to
determine which lymph nodes are invaded in patients who have a
particular tumor type. The aim of the RAMPS procedure is to
perform a complete N1 lymph node dissection and not resect N2
or N3 node levels. To do so, the position of N1 nodes had to be
dened, and we relied on anatomic studies of the lymphatic
drainage of the body of the pancreas (Fig. 3) as summarized in a
classic review by OMorchoe.8
The body and tail of the pancreas has 4 nearly equally
sized quadrants. Lymphatic vessels traveling from the 4 quad-
rants connect to lymphatics along the superior and inferior
borders of the gland.8 Small lymph nodes lie along the latter
lymphatics. The lymphatic vessels on the superior and inferior
borders of the left half of the body and tail drain to splenic
nodes in the splenic hilum or gastrosplenic nodes in the gas-
trosplenic omentum. Lymphatic vessels coursing along the su-
perior and inferior borders of the right half of the pancreatic
body drain to the gastroduodenal and infrapancreatic nodes.
These 4 sets of lymph nodes form a ring of nodes8 (Fig. 3). The
ring of nodes drain into nodes anterior to the aorta in relation to
the celiac and superior mesenteric arteries, but these nodes,
which may be thought of as a string of nodes, are not exclu-
sively an N2 node group. Lymphatics from the central part of
the pancreatic body enter these nodes directly without rst en-
tering a node on the ring.8 Therefore, they should be considered
as N1 as well as N2 nodes. Based on this information, an op-
eration designed to remove N1 nodes should resect both sets of
N1 nodes, which we have colloquially referred to as the ring
and the string of nodes.
Kayahara et al10 performed pathological mapping of lymph
nodes in cancer of the body and tail of the pancreas in 20
patients. Three node groups were involved in more than 20% of
patients: nodes along the superior and inferior borders of the
pancreas (nodes 11 and 18 in the Japanese system) and the
gastroduodenal node (node 8 in the Japanese system) (Fig. 3).
These are all resected in the RAMPS operation. Recently, Fujita
et al11 described the results of pathological lymph node mapping
in 50 patients with adenocarcinoma of the body and tail of the
pancreas. They identied a group of small lymph nodes attached
to the pancreas, seen only on histological slides. These nodes
were involved by the cancers in approximately 75% of patients.
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Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012

FIGURE 3. Lymphatic drainage of body and tail of pancreas. The ring of nodes are shown in boxes. The celiac and superior
mesenteric nodes make up the string of nodes. The gastroduodenal node is node 8 in the Japanese classification, whereas the node
chains on the superior and inferior borders are nodes 11 and 18. These nodes are most commonly involved in carcinoma of the body and
tail of the pancreas.

However, all other lymph node groups were involved very in-
frequently, usually in less than 10% of patients. The frequently
involved small lymph nodes may correspond to the nodes that
lie along the superior and inferior borders of the pancreas de-
scribed in OMorchoes study,8 although those were grossly
identiable as nodes. Whether these nodes are exactly the same
as those described by OMorchoe is uncertain, but they are cer-
tainly removed by RAMPS. The results of Fujita et al are inter-
esting, but it is unclear at present whether they apply to patients
in Western countries because the incidence of cancer in nodes
that could be macroscopically identied as lymph nodes grossly
was so low. In addition, as we will describe, Japanese patients
seem to have more well-differentiated tumors than American
patients, a fact that also suggests that the disease may differ sig-
nicantly in virulence in the 2 countries (United States vs Japan).
left limb is used. The abdomen is again explored for evidence of
metastases. The lesser sac is entered by freeing the omentum from
the colon or by opening through the gastrocolic ligament. The
gastrosplenic ligament is divided, taking the short gastric vessels
close to the stomach to remove the gastrosplenic node group. The
middle colic vein traced to the superior mesenteric vein. The neck
of the pancreas is elevated off the superior mesenteric and portal
veins. The right gastroepiploic vein may be sacriced if necessary
to display the superior mesenteric vein. A Kocher maneuver is
performed and the anterior surface of the left renal vein is exposed
for several centimeters. This will be useful later in the procedure
when the vein has to be identied on the left side.
The lesser omentum is opened, and the right gastric artery
is divided. The proper hepatic artery is identied and followed

Technique of the RAMPS Procedure

Preoperative Preparation
A recent abdominal CT scan is used to decide whether to
perform an anterior or posterior RAMPS.5 When a rim of nor-
mal pancreas remains posterior to the tumor, the anterior
RAMPS is chosen (Fig. 4). When the posterior margin of the
tumor contacts or seems to break through the posterior capsule
of the pancreas, the posterior RAMPS is selected (Fig. 5). The
tumor does not need to be seen to be touching or invading the
adrenal for a posterior RAMPS to be selected. It needs only to
be seen to have invaded posteriorly out of the pancreas. The
principle being applied is that the space between the back of the
pancreas and the front of the adrenal is too thin to reliably attain
negative margins when the tumor is present in the space. Of
course, in some instances, when the tumor is very far to the left
in the hilum of the spleen, it is well away from the adrenal. In
that, case it is the Gerota fascia and not the adrenal that needs to
be removed. FIGURE 4. Green line shows planned plane of posterior dissection
as shown in preoperative CT scan in anterior RAMPS in which
The Procedure the tumor has not penetrated the posterior capsule of the
pancreas. Note that the plane is on the anterior surface of the
Staging laparoscopy is performed to detect intra-abdominal adrenal. Red line shows possible plane when standard distal
metastases, which contraindicate the procedure. A left upper pancreatectomy is performed without regard to the position of the
quadrant J incision or Mercedes Benz incision with a longer anterior renal fascia. A indicates left adrenal gland; K, kidney.

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The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR

FIGURE 6. Anterior RAMPS at completion of dissection. White

numbers 1 to 4 show the 4 levels of the sagittal dissection:
1, pancreatic neck; 2, splenic vein; 3, side of celiac and SMA;
4, renal vein. A-C, Subsequent more coronal dissections: along the
adrenal vein (A), on the adrenal gland (B), along the surface of
Gerota fascia (C).
FIGURE 5. Green line shows planned plane of posterior dissection
as shown in preoperative CT scan in posterior RAMPS in which
the tumor has penetrated the posterior capsule of the pancreas.
A, left adrenal gland.
inferior attachments of the pancreas are divided as the dissec-
tion proceeds to the left. The inferior mesenteric vein is trans-
ected. Division of the lienorenal ligament is the last step in the
procedure. In the posterior RAMPS, the adrenal vein is divided at
proximally to display the common hepatic and gastroduodenal its termination into the left renal vein, and the dissection is carried
arteries. The gastroduodenal lymph node (node 8) is mobilized to the left and posteriorly behind the adrenal gland and onto the
from above downward and left, attached to the superior border surface of the kidney (Fig. 7). After removal from the patient, the
of the pancreas, as the common hepatic artery is displayed. The specimen is inked at the pancreatic neck margin and on the tan-
anterior surface of the portal vein is exposed by retracting gential margins using different colored inks, and a frozen section
the gastroduodenal artery (GDA) to the right. The neck of the of the neck of the pancreas is obtained.
pancreas is divided using a stapler. A celiac node dissection is These tumors may also invade several other organs or tis-
performed, taking all the nodes from the crus of the diaphragm sues in close relationship to the pancreas as described previ-
superiorly and posteriorly, off the celiac artery and the origins of ously (stomach, duodenum, and splenic exure of the colon).
the left gastric, hepatic, and splenic arteries. In this way, the Provided that the disease is local, any of these structures may be
origin of the splenic artery is exposed from a superior approach resected as in the standard method. The view at the end of the
as the celiac nodes are dissected downward. The celiac ganglia dissection in the 2 procedures is shown in Figures 6 and 7.
are not resected.
The splenic vein is isolated at its junction with the superior
mesenteric vein and divided with a vascular stapler. If tumor Laparoscopic Standard Distal Pancreatectomies and
invasion is present at this site, a resection of the superior mes- Laparoscopic RAMPS
enteric vein and/or portal vein is performed and repaired pri- Standard distal pancreatectomy has been performed suc-
marily or with a graft. The right border of the dissection is cessfully by minimally invasive techniques for more than a
carried downward in the sagittal plane, dividing fat and brous decade and has been applied to pancreatic carcinoma in some
tissue until the left side of the superior mesenteric artery is
identied (Fig. 6). The artery is followed on its left side, supe-
riorly and posteriorly, down to the aorta. The left sides of both
the superior mesenteric and celiac arteries should now be visible
down to the point that they come off the aorta. The lymph nodes
anterior to the aorta between the celiac artery and superior
mesenteric artery and those anterior and to the left of the su-
perior mesenteric artery are taken with this step.
The next step continues to develop the right border of
dissection, which is now carried in the sagittal plane through the
anterior renal fascia onto the renal and adrenal veins (Fig. 6).
This step is facilitated by placing a nger on the anterior surface
of the left renal vein behind the previously mobilized duode-
num. The nger can be palpated from the left side of the dis-
section posterior to the superior mesenteric artery. Dividing the
intervening tissue (anterior renal fascia) will expose the left
renal vein. In the anterior RAMPS, the adrenal vein is identied
and its anterior surface also becomes part of the posterior plane
of dissection, as does the anterior surface of the adrenal gland as
it is reached (Fig. 6). The dissection is continued in a postero- FIGURE 7. Posterior RAMPS at completion of dissection.
lateral direction onto the perinephric fat. The superior and Note the deeper level of dorsal dissection compared to Figure 6.

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Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012

centers. A large multi-institutional series found no difference in
survival between open and laparoscopic procedures.12 However,
the median follow-up time of 10 months was relatively short;
and the survival curve in the laparoscopic group, comprised of
only 23 patients, was somewhat immature, with only one patient
having reached 5 years of survival. The median survival in both
laparoscopic and open groups was 16 months.12
Theoretically, the RAMPS procedure can be performed
laparoscopically. The celiac node dissection and the formation
of the posterior plane right on the renal and adrenal veins will
be challenging, especially in large, deep patients. Fernandez-
Cruz et al13 reported results of a slightly modied RAMPS
procedure performed laparoscopically with good short-term
results, but survival was not addressed. Kang et al14 used a se-
lective approach, using laparoscopic resection when an anterior
RAMPS was indicated, but an open approach when a poste-
rior RAMPS was needed. One concern is that Kang et al and
Fernandez-Cruz et al seem to have performed a more limited
dissection with respect to the renal vein.13,14 In our technique,
we have assured that the plane of the posterior margin is behind
the anterior renal fascia by dissecting on to the left renal vein
and out along the surface of the adrenal vein. If this step is
omitted, it is possible that the plane will be too shallow and
anterior to the anterior renal fascia, risking an incomplete resection.
The number of patients requiring RAMPS is too small to
consider any kind of trial of open versus laparoscopic proce-
dure. Although the benets of laparoscopy are attractive, the
ability to complete the resection routinely without compromis-
ing the oncologic goals of the procedure is the primary con-
sideration. Therefore, at present, laparoscopic RAMPS should
be attempted in selected patients whose tumor and body habitus
are favorable; and the operation should be converted to open if
the oncologic principles are not being achieved.
patients had negative tangential margins. Four of 47 patients had a
positive margin at the pancreatic neck on permanent section, al-
though the frozen section diagnosis was negative for malignancy.
In all, 38 (81.0%) of 47 patients had negative margins.
Long-Term Survival
Mean and median follow-up times of living patients were
44.4 and 26.4 months, respectively. Eighteen patients (38.3%)
are alive, and 29 patients (61.7%) have died. Eleven patients
(23.4%) are alive without evidence of disease, and 7 patients
(14.8%) are alive with disease. Death occurred 1.4 to 74.4
months after surgical resection. Median survival was 25.9
months (Fig. 8). Five-year OS was 35.5% (Fig. 8). Seven
patients have lived longer than 5 years. The actual 5-year sur-
vival rate of the 23 patients whose surgery was performed more
than 5 years before the latest follow-up (June 30, 2010) was
30.4% (7/23). Judged by short-term outcome, number of nodes,
tangential margin negativity rate, and long-term survival, these
single-center results are very satisfactory.
Comparison of RAMPS With Standard
Distal Pancreatectomy
Pathologic and long-term outcomes of distal pancreatec-
tomies in other case series11,12,14Y26 are shown in Table 1. There
are many problems with comparing studies. Tangential margin
positivity rates are often reported, but inking of margins, which
makes the margin easier to evaluate by pathologists, does not

Results of the RAMPS Procedure

Surgical Outcome
We have recently reported our results in 47 patients who
underwent RAMPS for pancreatic adenocarcinoma between 1999
and 2008.5 The mean (SD) operative time was 243 (94) minutes.
Anterior RAMPS was performed in 32 patients and posterior
RAMPS with resection of the left adrenal gland in 15 patients.
Twenty-four patients underwent resection of 33 adjacent organs or
structures in addition to the left adrenal gland. There were no
postoperative (30 days) or inhospital deaths. Thirty-one patients
(66%) experienced 48 complications. The mean (SD) length of
postoperative hospital stay was 11.3 (6.8) days, and the mean (SD)
number of days in the ICU was 1.9 (2.5).

Pathological Results
Tumors ranged in diameter from 1.4 to 9.0 cm, with a
mean (SD) of 4.4 (2.1) cm. The mean (SD) number of lymph
nodes removed per patient was 18.0 (11.7), with a range of 1 to
60. Twenty-six (55%) of 47 patients had positive lymph nodes
in the resected specimen. Approximately one-half of the patients
had poorly differentiated tumors, and the other half had moderately
differentiated tumors (only one patient had a well-differentiated
tumor). Lymphovascular and perineural invasion were common.
American Joint Committee on Cancer staging of tumors included FIGURE 8. Overall survival results of RAMPS procedure. The
1 stage IA, 2 stage IB, 18 stage IIA, 24 stage IIB, 1 stage III, and curve is censored at 6 years, which is the time point beyond which
1 stage IV. One patient had adenocarcinoma arising within a cyst, fewer than 10% of patients have been followed. Hatch marks
and 2 patients had adenocarcinoma arising within a background of indicate censored patients within the 6-year follow-up period
intraductal papillary mucous neoplasm. Forty-two (89.3%) of 47 (reprinted from Mitchem et al5).

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The Cancer Journal & Volume 18, Number 6, November/December 2012 Left-Sided Pancreatectomies: RAMPS and DP-CAR

TABLE 1. Pathologic and Survival Data (Adapted from Mitchem et al5)

First Author Mean Tumor Percent Percent Grade Percent Mean Number of Median 5-Year
(Reference) Size (cm) N0/N1 W/M / P Margins R0/R1 Nodes Resected Survival (Mo) Survival (%)
Dalton15 5.0 73/27 NS R0 only NS 10 NS
Johnson16 NS 29/71 NS NS NS NS 14
Sperti17 5.5 75/25 58/29/12 NS NS 11 13
Kayahara18 NS 64/36 NS 36/64 NS NS 16
Burcharth19 4.3 39/61 23/23/54 77/23 NS 11 28*
Shoup20 4.7 51/49 0/62/38 72/28 NS 16 13
Christein21 5.5 36/64 2/76/22 78/22 NS 16 10
Shimada22 NS 21/79 29w/71mp 75/25 NS 22 (26)|| 19
Redmond23 4.3 55/45 NS 71/29 NS 16 16
Kooby12 4.4 46/54 NS 74/26 13 16 19
Kanda24 NS 49/51 12/76/12K 74/26 NS 13 6
Yamamoto25# 3.3 50/50 49/43/7 76/23 NS NS 30
Fujita11 4.0 40/60 28w/72mp** 90/10 31 23 19
Wu26 4.7 NS NS NS NS 15 0
Kang14# 4.2 66/44 18/69/12 87/13 NS 28 29
Mitchem (Authors series) 4.4 45/55 2/47/49 81/19 18 26 36
*Corrected for age-related deaths.
Authors estimation from survival of 2 groups.
Radial margins were assessed in only 62% of the patients.
mp, moderate plus poorly differentiated tumors.
||Includes 12 patients who had Appleby procedure. None of those patients survived more than 2 years, and the median survival in them was 17
months. Median survival excluding patients who had Appleby procedure was 26 months.
Results did not separate well-differentiated tumors from other grades.
#Used RAMPS technique in some patients in series.
**Ten other tumors were classied as papillary, mucinous, and adenosquamous.
Performed as part of a research study involving 2 pathologists who searched for subserosal lymph nodes along the body of the pancreas.
Includes results of all 50 patients in paper. These data were supplied in a personal communication by the authors.
Eighty-nine percent had negative tangential margins.

seem to have been done except in our study. The number of
lymph nodes resected is also reported infrequently.
Two studies from Asia (one from Korea14 and the other
from Japan25) have reported survival results similar to our own.
In both series, some patients were operated on using the
RAMPS approach. Excluding 12 patients who had tumors that
required resection of the celiac axis (modied Appleby proce-
dure), the results of Shimada et al22 who used a procedure that
was more radical than the posterior RAMPS are similar to ours.
One problem with comparing these results to our own is that the
reported grade of pancreatic carcinomas tend toward more well-
differentiated tumors in Japan11,22,24,25 and Korea14 than in
patients in case series from the United States. The survival
results of RAMPS seem to be better than the results reported
from Western centers using standard distal pancreatectomy in
the past, which have reported 5-year survival rates between 10%
and 19%.
Ideally, the RAMPS procedure should be tested against
standard distal pancreatectomy in a randomized trial. However,
this goal is likely not attainable because of the disparity between
the number of cases available for study and the number required
for a randomized trial. The median case per year per center is
3.4 in reported case series5 (Table 1). To compare 2 treatments
with 5-year survival of rates 20% and 35%, group sample sizes
of more than 200 patients would be required (i.e., a randomized
controlled trial to determine if RAMPS provides that level of
superior survival outcome would require a cooperative study
involving 25 or more high-volume pancreatic surgery centers
over several years. Available data are insufcient to comment
on the outcome of laparoscopic RAMPS.
DP-CAR
History of DP-CAR
In 1952, Lyon Appleby, a Canadian surgeon, presented a
case of gastrectomy with en bloc resection of the celiac and
common hepatic arteries in a patient with gastric adenocarci-
noma.27 In 1960, he presented a 10-year assessment of the op-
eration in his personal series of 19 cases.28 The liver maintained
its arterial blood supply by retrograde ow from the GDA via
the pancreatoduodenal arcade and the superior mesenteric ar-
tery (SMA) (Fig. 9). Since then, the Western literature has used
the eponymous term Appleby procedure to refer to any op-
eration for cancer that involves this strategy for resection of the
celiac axis and complete celiac lymph node clearance. As it has
been adapted for adenocarcinoma of the pancreas, a none-
ponymous term for the procedure is being used more frequently.
That term is radical distal (or left) pancreatectomy with resection
of the celiac axis, often shortened to DP-CAR, which in Asia
seems to be the preferred and customary term.
Anatomic Basis for DP-CAR
Distal pancreatectomy with celiac artery resection acutely
occludes the celiac artery, which deprives the liver of its normal

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Strasberg and Fields The Cancer Journal & Volume 18, Number 6, November/December 2012

FIGURE 9. Collateral pathway for blood supply to liver after DP-CAR. Tumor involves celiac and common hepatic arteries. Lines of
transection of these arteries are shown (red dashed lines). Blood supply depends on retrograde flow (red arrows) from the SMA, through
the inferior pancreatoduodenal artery and its branches and continues retrograde into the GDA through its branches. From there, the flow is
up the proper hepatic artery to the liver. This pathway also must supply the stomach by flow into the right gastric artery from the proper
hepatic artery and the right gastroepiploic artery through the GDA.

source of blood ow. It also deprives the stomach of blood
supply from its normal sources of blood ow. It is well known
that celiac artery occlusion from atherosclerotic disease does
not usually lead to hepatic infarction because of collateral cir-
culation from the SMA through the pancreatoduodenal arcade.
The inferior pancreatoduodenal artery (IPDA) arises from the
right side of the SMA 2 to 3 cm from its origin. Its anterior and
posterior branches (anterior and posterior inferior pancreato-
duodenal arteries) communicate with the anterior and posterior
branches of the GDA (anterior and posterior superior pancrea-
toduodenal arteries), and the whole makes up the pancreato-
duodenal arterial arcade that runs within the pancreas close to
the concave duodenal sweep (Fig. 9). The IPDA is often absent,
in which case, the anterior and posterior inferior pancreato-
duodenal arteries arise independently from the SMA. There are
many variations of this arterial anatomy, the description of
which is beyond the purpose of this paper. However, the critical
point is that the arcade is usually sufcient to support ow to the
liver when the common hepatic artery is occluded. Because of
concern that the ow might be insufcient when celiac artery
occlusion is abrupt, as in DP-CAR, some groups have embo-
lized the common hepatic artery with coils days or weeks before
the procedure. Others have simply placed a graft between the
aorta and the stump of the hepatic artery to avoid the problem of
hepatic ischemia.
Gastric ischemia has been a problem in some patients in most
case series. As the splenic artery is gone, there is no ow from the
left gastroepiploic or short gastric arteries, and ow must come
retrograde through the pancreatoduodenal arcade and into the right
gastric and right gastroepiploic arteries via the GDA.
Technique of DP-CAR
The technique is essentially that of an extended posterior
RAMPS procedure. The celiac artery origin is usually approached
from the right after an extensive mobilization of the duodenum.29
The SMA origin is also usually visible, and the IPDA origin can be
injured during the dissection to come around the celiac artery as
can the right renal artery. Therefore, great care must be taken to
avoid these complications. The celiac artery is divided at its origin
from the aorta and the common hepatic artery at its termination,
near the point where it branches into the GDA and proper hepatic
artery. If coils have been inserted into the common hepatic artery,
they are removed to facilitate the closure of the artery.29 After di-
vision of the celiac artery, the artery and the surrounding nerve
plexus is resected en bloc with the distal pancreas.
Results of DP-CAR
Distal pancreatectomy with celiac artery resection was
reported in 6 cases in 1997.30 The largest series of DP-CAR for
pancreatic adenocarcinoma comes from Hokkaido University in
Japan. These authors have presented their results in a series of
papers29,30Y34 In 2007, they reported on 23 patients who un-
derwent this operation between 1998 and 2005.33 No arterial
reconstructions were planned; however, 3 reconstructions were
necessary owing to intraoperative arterial injury requiring re-
vascularization. All operations included en bloc resection of the
celiac artery, common hepatic artery and left gastric artery, the
celiac plexus and ganglions, the nerve plexus around the SMA,
the crus of the diaphragm and Gerota fascia, the left adrenal
gland, the retroperitoneal fat above the left renal vein, the in-
ferior mesenteric vein, and all associated regional lymph nodes.
Preoperative coil embolization of the common hepatic artery was
described by this group33 and was performed in 19 patients
(83%) to encourage collateralization of hepatic arterial blood ow via
the GDA. Portal vein resection was performed in 16 patients (70%).
Eight patients (35%) underwent multi-visceral resection (4 gas-
tric resections, 3 colon resections, and 1 jejunal resection). On
pathologic analysis, all patients had invasive ductal adenocar-
cinoma of the pancreas. None had a carcinoma arising within or
in association with a mucinous cystic lesion. Following UICC
guidelines, all tumors were T3 or T4. Fifteen patients (65%) had
lymph node metastases. Twenty-one patients (91%) had an R0
resection. There were no postoperative deaths. The authors report
a 48% postoperative morbidity rate, including 4 pancreatic s-
tulas, and 3 cases of ischemic gastropathy. Two patients required
a second surgical procedure (one for ileus and one for intra-
peritoneal infection). The median survival after resection was
21.0 months, and the estimated 1- and 5- year OS rates were 71%

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The Cancer Journal & Volume 18, Number 6, November/December 2012
and 42%, respectively. Patterns of recurrence were not reported.
These results seem very encouraging. However, there are a
number of problems in evaluating the data. Importantly, the
Kaplan-Meier survival curves seem immature, with only one
patient having reached 5 years of survival.33 In subsequent
reports from this group, 5-year survival rates of 17%34 and
25%29 have been reported in this enlarging case series, sug-
gesting that the 5-year OS rate of 42% in the earlier report was
overly optimistic. Inking of the resected specimen does not seem
to have been routine. Actual invasion of the celiac and/or hepatic
arteries was present in only 2 patients but was more uniformly
present in surrounding nerve plexuses.
Hishinuma et al35 from the Tochigi Cancer Center in Japan
reported on 7 patients who had DP-CAR in an overall series
of 25 patients who underwent distal pancreatectomy for ade-
nocarcinoma from 1987 to 2003. Portal vein resection was
performed in one patient (14%). Six patients (86%) required
multi-visceral organ resection. All patients had ductal adeno-
carcinoma of the pancreas. All tumors were T3 or T4. Four
patients (57%) had lymph node metastases. Four patients
(57%) had an R0 resection. There were no postoperative
deaths. The authors report a 43% postoperative morbidity rate,
including one pancreatic stula. Survival rates are not deter-
minable from such small numbers. All patients have now died,
but one survived approximately 75 months and another sur-
vived approximately 45 months.
Shimada et al22 reported 12 patients who had DP-CAR as
part of a series of 88 patients who had a radical distal pancre-
atectomy similar to the posterior RAMPS. None of the 12 patients
lived more than 2 years. A number of other centers have reported
series with fewer cases of DP-CAR.36Y39
Evaluation of the Literature on DP-CAR
Distal pancreatectomy with celiac artery resection, unlike
RAMPS, is a true extended pancreatectomy. At present, it is ated treatment, including those who progress or are unable to
necessary to have serious reservations regarding the efcacy of
this procedure. Few patients have achieved long-term survival.
Our enthusiasm for new extended pancreatic procedures should
be tempered by the prior collective experience of extended
nodal and arterial resections for cancers of the head of the
pancreas. Therefore, DP-CAR should be conducted with me-
ticulous collection of data and detailed reporting. Of utmost
importance in interpreting results of DP-CAR is documentation
of pathologic evidence of celiac arterial invasion. This denes
the necessity of the operation: if there was no invasion of the
celiac artery, was the operation necessary? Of course, preoper-
ative and intraoperative determination of tumor invasion into
the celiac artery can be difcult, if not impossible. However, it
is critically important to report these data in such series. For
example, Hirano and Kondo report 18 (78%) of 23 patients with
perineural invasion of the nerve plexus surrounding the celiac
artery (CA), CHA, splenic artery (SA), and/or SMA; but only
two (9%) of these patients had intramural invasion of the CA or
CHA. It is unclear if clearing the perineural tissues around the
arteries would have been sufcient for an R0 resection, similar
to the strategy commonly used to clear the SMA during a
pancreaticoduodenectomy for adenocarcinoma of the head of
the pancreas.
Central to the question of the necessity of arterial resection
is the preoperative evaluation of patients with adenocarcinoma
of the body of the pancreas. In the reported DP-CAR literature,
this evaluation is not presented in much detail. It would be
important to correlate preoperative radiographic ndings and
postoperative pathologic ndings. Inking of resection speci-
mens is important in determining whether R0 resection has been
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Left-Sided Pancreatectomies: RAMPS and DP-CAR
attained. As discussed earlier, it may be difcult or impossible
to determine the necessity of arterial resection with a high de-
gree of certainty preoperatively, resulting in a low rate of true
arterial involvement, but a high degree of R0 resections.
Most of the reported series do not include patterns of
recurrence in their analyses. It is important to determine if
DP-CAR results in improved local control. This is especially
relevant given the low rate reported of true arterial invasion.
Might a lesser operation that includes dissection of the peri-
neural tissues from the celiac axis, followed by adjuvant ra-
diation therapy, lead to similar results? Because designing and
executing a trial to rigorously answer this question is likely
impossible, obtaining and documenting recurrence and adju-
vant treatment information in these patients is very relevant.
Patients with localized carcinoma of the body of the pan-
creas including those with involvement of the celiac axis should
be approached with curative intent, when possible. In such
patients, we currently prefer to begin with downsizing regi-
mens of chemotherapy, often with radiation therapy, for seve-
ral reasons. First, the current era of chemotherapy, including
FOLFIRINOX40 and other aggressive regimens, is effective in
achieving tumor regression, which may obviate the need for
arterial resection. Second, chemotherapy allows for patients
with aggressive biology to manifest metastatic spread before
surgery, thus sparing them the morbidity of aggressive surgery
with no potential for benet. Patients with locally advanced
nonmetastatic tumors are then appropriately selected for sur-
gery. Third, the addition of radiation may further allow for a
higher R0 resection rate, perhaps without arterial resection.
As such aggressive surgical approaches are used in the
modern era, detailed preoperative evaluation and postoperative
pathologic analysis should be reported to address these issues.
Furthermore, if patients are treated with downsizing strategies,
it is important to present the total number of patients that initi-
complete therapy. This allows for a proper determination of
the effectiveness of such protocols.
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